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1.  The Emergence of Environmental Homeostasis in Complex Ecosystems 
PLoS Computational Biology  2013;9(5):e1003050.
The Earth, with its core-driven magnetic field, convective mantle, mobile lid tectonics, oceans of liquid water, dynamic climate and abundant life is arguably the most complex system in the known universe. This system has exhibited stability in the sense of, bar a number of notable exceptions, surface temperature remaining within the bounds required for liquid water and so a significant biosphere. Explanations for this range from anthropic principles in which the Earth was essentially lucky, to homeostatic Gaia in which the abiotic and biotic components of the Earth system self-organise into homeostatic states that are robust to a wide range of external perturbations. Here we present results from a conceptual model that demonstrates the emergence of homeostasis as a consequence of the feedback loop operating between life and its environment. Formulating the model in terms of Gaussian processes allows the development of novel computational methods in order to provide solutions. We find that the stability of this system will typically increase then remain constant with an increase in biological diversity and that the number of attractors within the phase space exponentially increases with the number of environmental variables while the probability of the system being in an attractor that lies within prescribed boundaries decreases approximately linearly. We argue that the cybernetic concept of rein control provides insights into how this model system, and potentially any system that is comprised of biological to environmental feedback loops, self-organises into homeostatic states.
Author Summary
Life on Earth is perhaps greater than three and a half billion years old and it would appear that once it started it never stopped. During this period a number of dramatic shocks and drivers have affected the Earth. These include the impacts of massive asteroids, runaway climate change and increases in brightness of the Sun. Has life on Earth simply been lucky in withstanding such perturbations? Are there any self-regulating or homeostatic processes operating in the Earth system that would reduce the severity of such perturbations? If such planetary processes exist, to what extent are they the result of the actions of life? In this study, we show how the regulation of environmental conditions can emerge as a consequence of life's effects. If life is both affected by and affects it environment, then this coupled system can self-organise into a robust control system that was first described during the early cybernetics movement around the middle of the twentieth century. Our findings are in principle applicable to a wide range of real world systems - from microbial mats to aquatic ecosystems up to and including the entire biosphere.
doi:10.1371/journal.pcbi.1003050
PMCID: PMC3656095  PMID: 23696719
2.  Global analysis of river systems: from Earth system controls to Anthropocene syndromes. 
Continental aquatic systems from rivers to the coastal zone are considered within two perspectives: (i) as a major link between the atmosphere, pedosphere, biosphere and oceans within the Earth system with its Holocene dynamics, and (ii) as water and aquatic biota resources progressively used and transformed by humans. Human pressures have now reached a state where the continental aquatic systems can no longer be considered as being controlled by only Earth system processes, thus defining a new era, the Anthropocene. Riverine changes, now observed at the global scale, are described through a first set of syndromes (flood regulation, fragmentation, sediment imbalance, neo-arheism, salinization, chemical contamination, acidification, eutrophication and microbial contamination) with their related causes and symptoms. These syndromes have direct influences on water uses, either positive or negative. They also modify some Earth system key functions such as sediment, water, nutrient and carbon balances, greenhouse gas emissions and aquatic biodiversity. Evolution of river syndromes over the past 2000 years is complex: it depends upon the stages of regional human development and on natural conditions, as illustrated here for the chemical contamination syndrome. River damming, eutrophication and generalized decrease of river flow due to irrigation are some of the other global features of river changes. Future management of river systems should also consider these long-term impacts on the Earth system.
doi:10.1098/rstb.2003.1379
PMCID: PMC1693284  PMID: 14728790
3.  Widespread and persistent invasions of terrestrial habitats coincident with larval feeding behavior transitions during snail-killing fly evolution (Diptera: Sciomyzidae) 
Background
Transitions in habitats and feeding behaviors were fundamental to the diversification of life on Earth. There is ongoing debate regarding the typical directionality of transitions between aquatic and terrestrial habitats and the mechanisms responsible for the preponderance of terrestrial to aquatic transitions. Snail-killing flies (Diptera: Sciomyzidae) represent an excellent model system to study such transitions because their larvae display a range of feeding behaviors, being predators, parasitoids or saprophages of a variety of mollusks in freshwater, shoreline and dry terrestrial habitats. The remarkable genus Tetanocera (Tetanocerini) occupies five larval feeding groups and all of the habitat types mentioned above. This study has four principal objectives: (i) construct a robust estimate of phylogeny for Tetanocera and Tetanocerini, (ii) estimate the evolutionary transitions in larval feeding behaviors and habitats, (iii) test the monophyly of feeding groups and (iv) identify mechanisms underlying sciomyzid habitat and feeding behavior evolution.
Results
Bayesian inference and maximum likelihood analyses of molecular data provided strong support that the Sciomyzini, Tetanocerini and Tetanocera are monophyletic. However, the monophyly of many behavioral groupings was rejected via phylogenetic constraint analyses. We determined that (i) the ancestral sciomyzid lineage was terrestrial, (ii) there was a single terrestrial to aquatic habitat transition early in the evolution of the Tetanocerini and (iii) there were at least 10 independent aquatic to terrestrial habitat transitions and at least 15 feeding behavior transitions during tetanocerine phylogenesis. The ancestor of Tetanocera was aquatic with five lineages making independent transitions to terrestrial habitats and seven making independent transitions in feeding behaviors.
Conclusions
The preponderance of aquatic to terrestrial transitions in sciomyzids goes against the trend generally observed across eukaryotes. Damp shoreline habitats are likely transitional where larvae can change habitat but still have similar prey available. Transitioning from aquatic to terrestrial habitats is likely easier than the reverse for sciomyzids because morphological characters associated with air-breathing while under the water's surface are lost rather than gained, and sciomyzids originated and diversified during a general drying period in Earth's history. Our results imply that any animal lineage having aquatic and terrestrial members, respiring the same way in both habitats and having the same type of food available in both habitats could show a similar pattern of multiple independent habitat transitions coincident with changes in behavioral and morphological traits.
doi:10.1186/1471-2148-12-175
PMCID: PMC3483186  PMID: 22963084
4.  The Emergence and Early Evolution of Biological Carbon-Fixation 
PLoS Computational Biology  2012;8(4):e1002455.
The fixation of into living matter sustains all life on Earth, and embeds the biosphere within geochemistry. The six known chemical pathways used by extant organisms for this function are recognized to have overlaps, but their evolution is incompletely understood. Here we reconstruct the complete early evolutionary history of biological carbon-fixation, relating all modern pathways to a single ancestral form. We find that innovations in carbon-fixation were the foundation for most major early divergences in the tree of life. These findings are based on a novel method that fully integrates metabolic and phylogenetic constraints. Comparing gene-profiles across the metabolic cores of deep-branching organisms and requiring that they are capable of synthesizing all their biomass components leads to the surprising conclusion that the most common form for deep-branching autotrophic carbon-fixation combines two disconnected sub-networks, each supplying carbon to distinct biomass components. One of these is a linear folate-based pathway of reduction previously only recognized as a fixation route in the complete Wood-Ljungdahl pathway, but which more generally may exclude the final step of synthesizing acetyl-CoA. Using metabolic constraints we then reconstruct a “phylometabolic” tree with a high degree of parsimony that traces the evolution of complete carbon-fixation pathways, and has a clear structure down to the root. This tree requires few instances of lateral gene transfer or convergence, and instead suggests a simple evolutionary dynamic in which all divergences have primary environmental causes. Energy optimization and oxygen toxicity are the two strongest forces of selection. The root of this tree combines the reductive citric acid cycle and the Wood-Ljungdahl pathway into a single connected network. This linked network lacks the selective optimization of modern fixation pathways but its redundancy leads to a more robust topology, making it more plausible than any modern pathway as a primitive universal ancestral form.
Author Summary
The existence of the biosphere today depends on its capacity to fix inorganic into living matter. A wide range of evidence also suggests that the earliest life forms on Earth likewise derived their carbon from . From these two observations one can assume that the global biological carbon cycle has always been based on , and we show here that this assumption can be used as a powerful constraint to help organize and explain the deep evolution of life on Earth. Using a novel method that fully integrates aspects of metabolic and phylogenetic analysis, we are able to reconstruct the complete early evolutionary history of biological carbon-fixation, relating all ways in which life today performs this function to a single ancestral form. The diversification in carbon-fixation appears to underpin most of the deepest branches in the tree of life, and this early metabolic diversification – reaching back to the first cells – appears to have been driven not by the contingencies of history, but by direct links to the physical-chemical environment. The ancestral carbon-fixation pathway that we identify is different from any modern form, but better suited to the capabilities of the earliest primitive cells.
doi:10.1371/journal.pcbi.1002455
PMCID: PMC3334880  PMID: 22536150
5.  Implications of aquatic animal health for human health. 
Human health and aquatic animal health are organically related at three distinct interfaces. Aquatic animals serve as important contributors to the nutritional protein, lipid, and vitamin requirements of humans; as carriers and transmitters of many infectious and parasitic diseases to which humans are susceptible; and as indicators of toxic and carcinogenic substances that they can convey, in some part, from aquatic environments to man and other terrestrial animals. Transcending these relationships, but less visible and definable to many, is the role that aquatic animals play in the sustenance of our integrated planetary ecosystem. Up to the present, this ecosystem has been compatible with mankind's occupation of a niche within it at high but ultimately limited population levels. In the past century we have become clearly aware that human activities, particularly over-harvesting of aquatic animals together with chemical degradation of their habitats, can quite rapidly lead to perturbances that drastically shift aquatic ecosystems toward conditions of low productivity and impaired function as one of earth's vital organs. The negative values of aquatic animals as disease vectors are far outweighed by their positive values as nutritional sources and as sustainers of a relatively stable equilibrium in the global ecosystem. In the immediate future we can expect to see increased and improved monitoring of aquatic habitats to determine the extent to which aquatic animals cycle anthropogenic toxic and carcinogenic chemicals back to human consumers. In the long term, methods are particularly needed to assess the effects of these pollutants on reproductive success in aquatic communities and in human communities as well. As inputs of habitat-degrading substances change in quality and quantity, it becomes increasingly urgent to evaluate the consequences in advance, not in retrospect. A new, more realistic and comprehensive philosophy regarding aquatic environmental preservation and equally new and comprehensive technological advances reflective of this philosophy will be required. In the next century we will see a serious test of whether or not mankind has lost its ability to foresee and forestall the side effects of scientific and technological ingenuity.
PMCID: PMC1567767  PMID: 2205490
6.  A Tale of Two Oxidation States: Bacterial Colonization of Arsenic-Rich Environments 
PLoS Genetics  2007;3(4):e53.
Microbial biotransformations have a major impact on contamination by toxic elements, which threatens public health in developing and industrial countries. Finding a means of preserving natural environments—including ground and surface waters—from arsenic constitutes a major challenge facing modern society. Although this metalloid is ubiquitous on Earth, thus far no bacterium thriving in arsenic-contaminated environments has been fully characterized. In-depth exploration of the genome of the β-proteobacterium Herminiimonas arsenicoxydans with regard to physiology, genetics, and proteomics, revealed that it possesses heretofore unsuspected mechanisms for coping with arsenic. Aside from multiple biochemical processes such as arsenic oxidation, reduction, and efflux, H. arsenicoxydans also exhibits positive chemotaxis and motility towards arsenic and metalloid scavenging by exopolysaccharides. These observations demonstrate the existence of a novel strategy to efficiently colonize arsenic-rich environments, which extends beyond oxidoreduction reactions. Such a microbial mechanism of detoxification, which is possibly exploitable for bioremediation applications of contaminated sites, may have played a crucial role in the occupation of ancient ecological niches on earth.
Author Summary
Microorganisms play a crucial role in nutrient biogeochemical cycles. Arsenic is found throughout the environment from both natural and anthropogenic sources. Its inorganic forms are highly toxic and impair the physiology of most higher organisms. Arsenic contamination of groundwater supplies is giving rise to increasingly severe human health problems in both developing and industrial countries. In the present work, we investigated the metabolism of this metalloid in Herminiimonas arsenicoxydans, a representative organism of a novel bacterial genus widespread in aquatic environments. Examination of the genome sequence and experimental evidence revealed that it is remarkably capable of coping with arsenic. Our observations support the existence of multiple strategies allowing arsenic-metabolizing microbes to efficiently colonize toxic environments. In particular, arsenic oxidation and scavenging may have played a crucial role in the development of early stages of life on Earth. Such mechanisms may one day be exploited as part of a potential bioremediation strategy in toxic environments.
doi:10.1371/journal.pgen.0030053
PMCID: PMC1851979  PMID: 17432936
7.  Rod Monochromacy and the Coevolution of Cetacean Retinal Opsins 
PLoS Genetics  2013;9(4):e1003432.
Cetaceans have a long history of commitment to a fully aquatic lifestyle that extends back to the Eocene. Extant species have evolved a spectacular array of adaptations in conjunction with their deployment into a diverse array of aquatic habitats. Sensory systems are among those that have experienced radical transformations in the evolutionary history of this clade. In the case of vision, previous studies have demonstrated important changes in the genes encoding rod opsin (RH1), short-wavelength sensitive opsin 1 (SWS1), and long-wavelength sensitive opsin (LWS) in selected cetaceans, but have not examined the full complement of opsin genes across the complete range of cetacean families. Here, we report protein-coding sequences for RH1 and both color opsin genes (SWS1, LWS) from representatives of all extant cetacean families. We examine competing hypotheses pertaining to the timing of blue shifts in RH1 relative to SWS1 inactivation in the early history of Cetacea, and we test the hypothesis that some cetaceans are rod monochomats. Molecular evolutionary analyses contradict the “coastal” hypothesis, wherein SWS1 was pseudogenized in the common ancestor of Cetacea, and instead suggest that RH1 was blue-shifted in the common ancestor of Cetacea before SWS1 was independently knocked out in baleen whales (Mysticeti) and in toothed whales (Odontoceti). Further, molecular evidence implies that LWS was inactivated convergently on at least five occasions in Cetacea: (1) Balaenidae (bowhead and right whales), (2) Balaenopteroidea (rorquals plus gray whale), (3) Mesoplodon bidens (Sowerby's beaked whale), (4) Physeter macrocephalus (giant sperm whale), and (5) Kogia breviceps (pygmy sperm whale). All of these cetaceans are known to dive to depths of at least 100 m where the underwater light field is dim and dominated by blue light. The knockout of both SWS1 and LWS in multiple cetacean lineages renders these taxa rod monochromats, a condition previously unknown among mammalian species.
Author Summary
The emergence of Cetacea (whales, dolphins, porpoises) represents a profound transition in the history of life. Living cetaceans have evolved a spectacular array of adaptations in association with their return to aquatic habitats. Aquatic environments impose challenging constraints on sensory systems, including vision, and the cetacean eye exhibits both anatomical and molecular specializations that enhance underwater sight. Most mammals have one photopigment (RH1) for dim-light vision and two photopigments (long wavelength-sensitive opsin [LWS], short wavelength-sensitive opsin [SWS1]) for daytime, color vision. By contrast, cetaceans have an inactivated copy of the gene that encodes SWS1. Here, we show that LWS is also inactivated in several cetacean lineages including the giant sperm whale, Sowerby's beaked whale, and balaenopteroids (rorquals plus gray whale). These cetaceans dive to depths of at least 100 meters where the underwater light field is dominated by dim, blue light. The knockout of both cone pigments renders these taxa rod monochromats, a condition that is previously unknown among mammalian species. Rod opsin remains functional in these taxa and is blue-shifted to increase its sensitivity to the available blue light that occurs in deep water conditions. These results further elucidate the molecular blueprint of modern cetacean species.
doi:10.1371/journal.pgen.1003432
PMCID: PMC3630094  PMID: 23637615
8.  Early anaerobic metabolisms 
Before the advent of oxygenic photosynthesis, the biosphere was driven by anaerobic metabolisms. We catalogue and quantify the source strengths of the most probable electron donors and electron acceptors that would have been available to fuel early-Earth ecosystems. The most active ecosystems were probably driven by the cycling of H2 and Fe2+ through primary production conducted by anoxygenic phototrophs. Interesting and dynamic ecosystems would have also been driven by the microbial cycling of sulphur and nitrogen species, but their activity levels were probably not so great. Despite the diversity of potential early ecosystems, rates of primary production in the early-Earth anaerobic biosphere were probably well below those rates observed in the marine environment. We shift our attention to the Earth environment at 3.8 Gyr ago, where the earliest marine sediments are preserved. We calculate, consistent with the carbon isotope record and other considerations of the carbon cycle, that marine rates of primary production at this time were probably an order of magnitude (or more) less than today. We conclude that the flux of reduced species to the Earth surface at this time may have been sufficient to drive anaerobic ecosystems of sufficient activity to be consistent with the carbon isotope record. Conversely, an ecosystem based on oxygenic photosynthesis was also possible with complete removal of the oxygen by reaction with reduced species from the mantle.
doi:10.1098/rstb.2006.1906
PMCID: PMC1664682  PMID: 17008221
Archaean; evolution; hydrogen; anoxygenic photosynthesis; iron; metabolism
9.  Secondary Ultraweak Luminescence from Humic Acids Induced by γ-Radiation 
Humic substances (HSs) are products of biochemical transformations of plant and animal residues that make up a major fraction of the organic carbon of soil and aquatic systems in the environment. Because radioisotopes occur in the Earth’s crust and because the entire biosphere is continuously exposed to cosmic radiation, ionizing radiation continually interacts with HSs. This chronic irradiation could have a significant ecological impact. However, very few publications are available that address possible consequences of chronic exposure of HSs to ionizing radiation from terrestrial and cosmic sources. This study was conducted to investigate possible impacts of exposure of HSs to ionizing radiation.
Dried humic acid (HA) or its associated aqueous solution (in 0.1 M Na2CO3) were exposed to absorbed γ-radiation in high doses of 1–90 kGy using a 60Co source. Following the γ-ray exposures, a secondary, ultraweak radiation emanation with wavelengths in the spectral range λ= 340–650 nm was recorded as a long-lived chemiluminescence (CL) from the aqueous solutions; however, the CL was not observed after irradiating dry HA.
Absorption spectra (for λ=240–800 nm) of irradiated solutions indicated that polymerization/degradation processes were operating on the HA macromolecules. The effect of specific CL enhancers (luminol and lucigenin) on the intensity and kinetics of the CL implicated the participation of reactive oxygen species and free radicals in the CL and polymerization/degradation processes. For the range of absorbed doses used (1–10 kGy), the intensity of the induced CL was nonlinearly related to dose, suggesting that complex radical formation mechanisms were involved.
doi:10.1080/15401420490507468
PMCID: PMC2657483  PMID: 19330147
humic acid; luminescence; γ-irradiation
10.  Transport and transportation pathways of hazardous chemicals from solid waste disposal. 
To evaluate the impact of hazardous chemicals in solid wastes on man and other organisms, it is necessary to have information about amounts of chemical present, extent of exposure, and chemical toxicity. This paper addresses the question of organism exposure by considering the major physical and biological transport pathways and the physicochemical and biochemical transformations that may occur in sediments, soils, and water. Disposal of solid wastes in both terrestrial and oceanic environments is considered. Atmospheric transport is considered for emissions from incineration of solid wastes and for wind resuspension of particulates from surface waste deposits. Solid wastes deposited in terrestrial environments are subject to leaching by surface and ground waters. Leachates may then be transported to other surface waters and drinking water aquifers through hydrologic transport. Leachates also interact with natural organic matter, clays, and microorganisms in soils and sediments. These interactions may render chemical constituents in leachates more or less mobile, possibly change chemical and physical forms, and alter their biological activity. Oceanic waste disposal practices result in migration through diffusion and ocean currents. Surface area-to-volume ratios play a major role in the initial distributions of chemicals in the aquatic environment. Sediments serve as major sources and sinks of chemical contaminants. Food chain transport in both aquatic and terrestrial environments results in the movement of hazardous chemicals from lower to higher positions in the food web. Bioconcentration is observed in both terrestrial and aquatic food chains with certain elements and synthetic organics. Bioconcentration factors tend to be higher for synthetic organics, and higher in aquatic than in terrestrial systems. Biodilution is not atypical in terrestrial environments. Synergistic and antagonistic actions are common occurrences among chemical contaminants and can be particularly important toxicity considerations in aquatic environments receiving runoff from several terrestrial sources.
PMCID: PMC1637272  PMID: 367772
11.  Adaptive evolution and functional constraint at TLR4 during the secondary aquatic adaptation and diversification of cetaceans 
Background
Cetaceans (whales, dolphins and porpoises) are a group of adapted marine mammals with an enigmatic history of transition from terrestrial to full aquatic habitat and rapid radiation in waters around the world. Throughout this evolution, the pathogen stress-response proteins must have faced challenges from the dramatic change of environmental pathogens in the completely different ecological niches cetaceans occupied. For this reason, cetaceans could be one of the most ideal candidate taxa for studying evolutionary process and associated driving mechanism of vertebrate innate immune systems such as Toll-like receptors (TLRs), which are located at the direct interface between the host and the microbial environment, act at the first line in recognizing specific conserved components of microorganisms, and translate them rapidly into a defense reaction.
Results
We used TLR4 as an example to test whether this traditionally regarded pattern recognition receptor molecule was driven by positive selection across cetacean evolutionary history. Overall, the lineage-specific selection test showed that the dN/dS (ω) values along most (30 out of 33) examined cetartiodactylan lineages were less than 1, suggesting a common effect of functional constraint. However, some specific codons made radical changes, fell adjacent to the residues interacting with lipopolysaccharides (LPS), and showed parallel evolution between independent lineages, suggesting that TLR4 was under positive selection. Especially, strong signatures of adaptive evolution on TLR4 were identified in two periods, one corresponding to the early evolutionary transition of the terrestrial ancestors of cetaceans from land to semi-aquatic (represented by the branch leading to whale + hippo) and from semi-aquatic to full aquatic (represented by the ancestral branch leading to cetaceans) habitat, and the other to the rapid diversification and radiation of oceanic dolphins.
Conclusions
This is the first study thus far to characterize the TLR gene in cetaceans. Our data present evidences that cetacean TLR4 has undergone adaptive evolution against the background of purifying selection in response to the secondary aquatic adaptation and rapid diversification in the sea. It is suggested that microbial pathogens in different environments are important factors that promote adaptive changes at cetacean TLR4 and new functions of some amino acid sites specialized for recognizing pathogens in dramatically contrasted environments to enhance the fitness for the adaptation and survival of cetaceans.
doi:10.1186/1471-2148-12-39
PMCID: PMC3384459  PMID: 22443485
12.  The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria 
eLife  2013;2:e01102.
Cyanobacteria were responsible for the oxygenation of the ancient atmosphere; however, the evolution of this phylum is enigmatic, as relatives have not been characterized. Here we use whole genome reconstruction of human fecal and subsurface aquifer metagenomic samples to obtain complete genomes for members of a new candidate phylum sibling to Cyanobacteria, for which we propose the designation ‘Melainabacteria’. Metabolic analysis suggests that the ancestors to both lineages were non-photosynthetic, anaerobic, motile, and obligately fermentative. Cyanobacterial light sensing may have been facilitated by regulators present in the ancestor of these lineages. The subsurface organism has the capacity for nitrogen fixation using a nitrogenase distinct from that in Cyanobacteria, suggesting nitrogen fixation evolved separately in the two lineages. We hypothesize that Cyanobacteria split from Melainabacteria prior or due to the acquisition of oxygenic photosynthesis. Melainabacteria remained in anoxic zones and differentiated by niche adaptation, including for symbiosis in the mammalian gut.
DOI: http://dx.doi.org/10.7554/eLife.01102.001
eLife digest
Microbes are ubiquitous in the world and exist in complex communities called microbiomes that have colonized many environments, including the human gut. Until modern techniques for sequencing nucleic acids became available, many of the organisms found in these microbiomes could not be studied because they could not be cultured in the laboratory. However, advances in sequencing technology have made it possible to study the evolution and properties of these microbes, including their impact on human health.
Bacteria belonging to the phylum Cyanobacteria had a significant effect on the prehistoric Earth because they were the first organisms to produce gaseous oxygen as a byproduct of photosynthesis, and thus shaped the Earth’s oxygen-rich atmosphere. Early plants took up these bacteria in a symbiotic relationship, and plastids—the organelles in plant cells that perform photosynthesis and produce oxygen–are the descendants of Cyanobacteria.
Organisms evolutionarily related to Cyanobacteria have been found in the human gut and in various aquatic sources, but these bacteria have not been studied because it has not been possible to isolate or culture them. Now, Di Rienzi, Sharon et al. have used modern sequencing techniques to obtain complete genomes for some of these bacteria, which they assign to a new phylum called Melainabacteria.
By analyzing these genomes, Di Rienzi, Sharon et al. were able to make predictions about the cell structure and metabolic abilities of Melainabacteria. Like Cyanobacteria, they have two membranes surrounding the bacterial cell; unlike Cyanobacteria, however, they have flagella that propel them through liquid or across surfaces. Most interestingly, Melainabacteria are not able to perform photosynthesis, but instead produce energy through fermentation and release hydrogen gas that can be consumed by other microorganisms.
The genome of the bacteria isolated from water reveals that it has the capacity to fix nitrogen. Cyanobacteria can also fix atmospheric nitrogen, but the protein complexes used by the two phyla are not related, which suggests that nitrogen fixation evolved after the evolutionary divergence of Cyanobacteria and Melainabacteria.
By exploring previously published datasets of bacterial communities, Di Rienzi, Sharon et al. found that Melainabacteria are common in aquatic habitats. They are also prevalent in the guts of herbivorous mammals and humans with a predominantly vegetarian diet. Melainabacteria from the human gut also synthesize several B and K vitamins, which suggests that these bacteria are beneficial to their host because in addition to aiding with the digestion of plant fibers, they are also a source of vitamins.
DOI: http://dx.doi.org/10.7554/eLife.01102.002
doi:10.7554/eLife.01102
PMCID: PMC3787301  PMID: 24137540
Cyanobacteria; Melainabacteria; photosynthesis; nitrogen fixation; human gut; subsurface; Human; Other
13.  New insights into the evolutionary history of biological nitrogen fixation 
Nitrogenase, which catalyzes the ATP-dependent reduction of dinitrogen (N2) to ammonia (NH3), accounts for roughly half of the bioavailable nitrogen supporting extant life. The fundamental requirement for fixed forms of nitrogen for life on Earth, both at present and in the past, has led to broad and significant interest in the origin and evolution of biological N2 fixation. One key question is whether the limited availability of fixed nitrogen was a factor in life's origin or whether there were ample sources of fixed nitrogen produced by abiotic processes or delivered through the weathering of bolide impact materials to support this early life. If the latter, the key questions become what were the characteristics of the environment that precipitated the evolution of this oxygen sensitive process, when did this occur, and how was its subsequent evolutionary history impacted by the advent of oxygenic photosynthesis and the rise of oxygen in the Earth's biosphere. Since the availability of fixed sources of nitrogen capable of supporting early life is difficult to glean from the geologic record, there are limited means to get direct insights into these questions. Indirect insights, however, can be gained through phylogenetic studies of nitrogenase structural gene products and additional gene products involved in the biosynthesis of the complex metal-containing prosthetic groups associated with this enzyme complex. Insights gained from such studies, as reviewed herein, challenge traditional models for the evolution of biological nitrogen fixation and provide the basis for the development of new conceptual models that explain the stepwise evolution of this highly complex life sustaining process.
doi:10.3389/fmicb.2013.00201
PMCID: PMC3733012  PMID: 23935594
nitrogen fixation; great oxidation event; NIf; methanogens
14.  Pollutant Dehalogenation Capability May Depend on the Trophic Evolutionary History of the Organism: PBDEs in Freshwater Food Webs 
PLoS ONE  2012;7(7):e41829.
Organohalogen compounds are some of the most notorious persistent pollutants disturbing the Earth biosphere. Although human-made, these chemicals are not completely alien to living systems. A large number of natural organohalogens, part of the secondary metabolism, are involved in chemical trophic interactions. Surprisingly, the relationship between organisms’ trophic position and synthetic organohalogen biotransformation capability has not been investigated. We studied the case for polybromodiphenyl ethers (PBDE), a group of flame-retardants of widespread use in the recent years, in aquatic food webs from remote mountain lakes. These relatively simple ecosystems only receive pollution by atmospheric transport. A large predominance of the PBDE congener currently in use in Europe, BDE-209, largely dominated the PBDE composition of the basal resources of the food web. In contrast, primary consumers (herbivores and detritivores) showed a low proportion of BDE-209, and dominance of several less brominated congeners (e.g. BDE-100, BDE47). Secondary consumers (predators) showed large biomagnification of BDE-209 compare to other congeners. Finally, top predator fish characterized by low total PBDE concentrations. Examination of the bromine stable isotopic composition indicates that primary consumers showed higher PBDE biotransformation capability than secondary consumers. We suggest that the evolutionary response of primary consumers to feeding deterrents would have pre-adapted them for PBDE biotransformation. The observed few exceptions, some insect taxa, can be interpreted in the light of the trophic history of the evolutionary lineage of the organisms. Bromine isotopic composition in fish indicates that low PBDE values are due to not only biotransformation but also to some other process likely related to transport. Our finding illustrates that organohalogen compounds may strongly disturb ecosystems even at low concentrations, since the species lacking or having scarce biotransformation capability may be selectively more exposed to these halogenated hydrophobic semi-volatile organic pollutants due to their high bioaccumulation potential.
doi:10.1371/journal.pone.0041829
PMCID: PMC3407054  PMID: 22848624
15.  Protection against Mycobacterium ulcerans Lesion Development by Exposure to Aquatic Insect Saliva 
PLoS Medicine  2007;4(2):e64.
Background
Buruli ulcer is a severe human skin disease caused by Mycobacterium ulcerans. This disease is primarily diagnosed in West Africa with increasing incidence. Antimycobacterial drug therapy is relatively effective during the preulcerative stage of the disease, but surgical excision of lesions with skin grafting is often the ultimate treatment. The mode of transmission of this Mycobacterium species remains a matter of debate, and relevant interventions to prevent this disease lack (i) the proper understanding of the M. ulcerans life history traits in its natural aquatic ecosystem and (ii) immune signatures that could be correlates of protection. We previously set up a laboratory ecosystem with predatory aquatic insects of the family Naucoridae and laboratory mice and showed that (i) M. ulcerans-carrying aquatic insects can transmit the mycobacterium through bites and (ii) that their salivary glands are the only tissues hosting replicative M. ulcerans. Further investigation in natural settings revealed that 5%–10% of these aquatic insects captured in endemic areas have M. ulcerans–loaded salivary glands. In search of novel epidemiological features we noticed that individuals working close to aquatic environments inhabited by insect predators were less prone to developing Buruli ulcers than their relatives. Thus we set out to investigate whether those individuals might display any immune signatures of exposure to M. ulcerans-free insect predator bites, and whether those could correlate with protection.
Methods and Findings
We took a two-pronged approach in this study, first investigating whether the insect bites are protective in a mouse model, and subsequently looking for possibly protective immune signatures in humans. We found that, in contrast to control BALB/c mice, BALB/c mice exposed to Naucoris aquatic insect bites or sensitized to Naucoris salivary gland homogenates (SGHs) displayed no lesion at the site of inoculation of M. ulcerans coated with Naucoris SGH components. Then using human serum samples collected in a Buruli ulcer–endemic area (in the Republic of Benin, West Africa), we assayed sera collected from either ulcer-free individuals or patients with Buruli ulcers for the titre of IgGs that bind to insect predator SGH, focusing on those molecules otherwise shown to be retained by M. ulcerans colonies. IgG titres were lower in the Buruli ulcer patient group than in the ulcer-free group.
Conclusions
These data will help structure future investigations in Buruli ulcer–endemic areas, providing a rationale for research into human immune signatures of exposure to predatory aquatic insects, with special attention to those insect saliva molecules that bind to M. ulcerans.
Saliva from aquatic insects in areas where Buruli ulcer is endemic can protect mice against the disease's characteristic skin lesion and might play a role in natural immunity in humans.
Editors' Summary
Background.
Buruli ulcer disease is a severe skin infection caused by Mycobacterium ulcerans, a bacterium related to those that cause tuberculosis and leprosy. This poorly understood disease affects people living near slow-flowing or standing water in poor rural communities in tropical and subtropical countries. How people become infected with M. ulcerans is unclear but one possibility is that infected aquatic insects transmit it through their bites. The first sign of infection is usually a small painless swelling in the skin. Bacteria inside these swellings produce a toxin that damages nearby soft tissues until eventually the skin sloughs off to leave a large open sore. This usually heals but the resultant scar can limit limb movement. Consequently, 25% of people affected by Buruli ulcers—most of whom are children—are permanently disabled. If the disease is caught early, powerful antibiotics can prevent ulcer formation. But most patients do not seek help until the later stages when the only treatment is to cut out the infection and do a skin graft, a costly and lengthy treatment.
Why Was This Study Done?
There is currently no effective way to prevent Buruli ulcers. To develop an effective preventative strategy, researchers need to determine exactly how the infection is transmitted to people and what makes some individuals resistant to infection. Previous studies have indicated that 5%–10% of some aquatic insect predators that live in areas where Buruli ulcers occur have M. ulcerans in their salivary glands and that aquatic insects carrying M. ulcerans can transmit it to mice through bites. Furthermore, people working close to water inhabited by insect predators are less likely to develop Buruli ulcers than their relatives who do not work near water. In this study, therefore, the researchers investigated whether exposure to noninfected insect saliva provides some protection against M. ulcerans infection.
What Did the Researchers Do and Find?
The researchers let uninfected aquatic insects bite ten mice several times before exposing these mice and ten unbitten mice to M. ulcerans-infected water bugs. Only one pre-bitten mouse developed an M. ulcerans-containing lesion compared with eight control mice. Next, the researchers injected mice with insect salivary gland extracts before challenging them with “naked” M. ulcerans or bacteria coated with salivary gland extract. Most uninjected mice developed lesions when challenged with coated or naked M. ulcerans, as did experimental mice challenged with naked M. ulcerans. However, most experimental mice challenged with coated M. ulcerans remained lesion-free. In both experiments, the blood of the pre-bitten and extract-treated mice (but not the control mice) contained antibodies (immune system proteins that provide protection against infections and foreign proteins) to proteins in insect salivary gland extracts that stick to M. ulcerans. Finally, the researchers measured the blood concentration (the titer) of antibodies that bind insect salivary gland proteins in patients with Buruli ulcer and in healthy people living in the same area. People with high titers of these antibodies, they report, were less likely to have Buruli ulcers than those with low titers.
What Do These Findings Mean?
These findings suggest that exposure to aquatic insect saliva may provide some protection against M. ulcerans lesion development. However, the current results have several limitations. In particular they will only be relevant to human disease if M. ulcerans is normally transmitted by insect bites, and this has not been proven yet. Also, because the human study did not measure the overall immune status of the study participants, the people with Buruli ulcers may have had a general immune deficit rather than simply lacking antibodies against insect salivary gland proteins. However, if the human findings can be repeated and expanded, they suggest that low antibody titers to salivary gland proteins might identify those people who are most susceptible to M ulcerans infections and who would thus benefit most from regular tests for early signs of the disease. Finally, further work on the immune mechanism by which exposure to insect salivary gland proteins protects against M. ulcerans infections may help in the development of vaccines against Buruli ulcer disease.
Additional Information.
Please access these Web sites via the online version of this summary at http://dx.doi.org/10.1371/journal.pmed.0040064.
A related PLoS Medicine Perspective article by Manuel T. Silva and others discusses this study and others on insect-borne parasitic diseases
World Health Organization has information on Buruli ulcer disease
US Centers for Disease Control and Prevention has information on Buruli ulcer
The US Armed Forces Institute of Pathology Web site contains pages on Buruli ulcer
Leprosy Relief Emmaus Switzerland offers information on Buruli ulcer
Wikipedia contains pages on Buruli ulcer (note: Wikipedia is an online encyclopedia that anyone can edit)
PLoS Medicine has a detailed review article on Buruli ulcer by Paul D. R. Johnson and colleagues
doi:10.1371/journal.pmed.0040064
PMCID: PMC1808094  PMID: 17326707
16.  Emerging viral diseases of fish and shrimp 
Veterinary Research  2010;41(6):51.
The rise of aquaculture has been one of the most profound changes in global food production of the past 100 years. Driven by population growth, rising demand for seafood and a levelling of production from capture fisheries, the practice of farming aquatic animals has expanded rapidly to become a major global industry. Aquaculture is now integral to the economies of many countries. It has provided employment and been a major driver of socio-economic development in poor rural and coastal communities, particularly in Asia, and has relieved pressure on the sustainability of the natural harvest from our rivers, lakes and oceans. However, the rapid growth of aquaculture has also been the source of anthropogenic change on a massive scale. Aquatic animals have been displaced from their natural environment, cultured in high density, exposed to environmental stress, provided artificial or unnatural feeds, and a prolific global trade has developed in both live aquatic animals and their products. At the same time, over-exploitation of fisheries and anthropogenic stress on aquatic ecosystems has placed pressure on wild fish populations. Not surprisingly, the consequence has been the emergence and spread of an increasing array of new diseases. This review examines the rise and characteristics of aquaculture, the major viral pathogens of fish and shrimp and their impacts, and the particular characteristics of disease emergence in an aquatic, rather than terrestrial, context. It also considers the potential for future disease emergence in aquatic animals as aquaculture continues to expand and faces the challenges presented by climate change.
doi:10.1051/vetres/2010022
PMCID: PMC2878170  PMID: 20409453
disease emergence; shrimp; fish; virus
17.  Pharmaceuticals and personal care products in the environment: agents of subtle change? 
Environmental Health Perspectives  1999;107(Suppl 6):907-938.
During the last three decades, the impact of chemical pollution has focused almost exclusively on the conventional "priority" pollutants, especially those acutely toxic/carcinogenic pesticides and industrial intermediates displaying persistence in the environment. This spectrum of chemicals, however, is only one piece of the larger puzzle in "holistic" risk assessment. Another diverse group of bioactive chemicals receiving comparatively little attention as potential environmental pollutants includes the pharmaceuticals and active ingredients in personal care products (in this review collectively termed PPCPs), both human and veterinary, including not just prescription drugs and biologics, but also diagnostic agents, "nutraceuticals," fragrances, sun-screen agents, and numerous others. These compounds and their bioactive metabolites can be continually introduced to the aquatic environment as complex mixtures via a number of routes but primarily by both untreated and treated sewage. Aquatic pollution is particularly troublesome because aquatic organisms are captive to continual life-cycle, multigenerational exposure. The possibility for continual but undetectable or unnoticed effects on aquatic organisms is particularly worrisome because effects could accumulate so slowly that major change goes undetected until the cumulative level of these effects finally cascades to irreversible change--change that would otherwise be attributed to natural adaptation or ecologic succession. As opposed to the conventional, persistent priority pollutants, PPCPs need not be persistent if they are continually introduced to surface waters, even at low parts-per-trillion/parts-per-billion concentrations (ng-microg/L). Even though some PPCPs are extremely persistent and introduced to the environment in very high quantities and perhaps have already gained ubiquity worldwide, others could act as if they were persistent, simply because their continual infusion into the aquatic environment serves to sustain perpetual life-cycle exposures for aquatic organisms. This review attempts to synthesize the literature on environmental origin, distribution/occurrence, and effects and to catalyze a more focused discussion in the environmental science community.
PMCID: PMC1566206  PMID: 10592150
18.  The carbon cycle on early Earth—and on Mars? 
One of the goals of the present Martian exploration is to search for evidence of extinct (or even extant) life. This could be redefined as a search for carbon. The carbon cycle (or, more properly, cycles) on Earth is a complex interaction among three reservoirs: the atmosphere; the hydrosphere; and the lithosphere. Superimposed on this is the biosphere, and its presence influences the fixing and release of carbon in these reservoirs over different time-scales. The overall carbon balance is kept at equilibrium on the surface by a combination of tectonic processes (which bury carbon), volcanism (which releases it) and biology (which mediates it). In contrast to Earth, Mars presently has no active tectonic system; neither does it possess a significant biosphere. However, these observations might not necessarily have held in the past. By looking at how Earth's carbon cycles have changed with time, as both the Earth's tectonic structure and a more sophisticated biology have evolved, and also by constructing a carbon cycle for Mars based on the carbon chemistry of Martian meteorites, we investigate whether or not there is evidence for a Martian biosphere.
doi:10.1098/rstb.2006.1898
PMCID: PMC1664679  PMID: 17008211
Earth; Mars; carbon; cycle; life
19.  Warming will affect phytoplankton differently: evidence through a mechanistic approach 
Although the consequences of global warming in aquatic ecosystems are only beginning to be revealed, a key to forecasting the impact on aquatic communities is an understanding of individual species' vulnerability to increased temperature. Despite their microscopic size, phytoplankton support about half of the global primary production, drive essential biogeochemical cycles and represent the basis of the aquatic food web. At present, it is known that phytoplankton are important targets and, consequently, harbingers of climate change in aquatic systems. Therefore, investigating the capacity of phytoplankton to adapt to the predicted warming has become a relevant issue. However, considering the polyphyletic complexity of the phytoplankton community, different responses to increased temperature are expected. We experimentally tested the effects of warming on 12 species of phytoplankton isolated from a variety of environments by using a mechanistic approach able to assess evolutionary adaptation (the so-called ratchet technique). We found different degrees of tolerance to temperature rises and an interspecific capacity for genetic adaptation. The thermal resistance level reached by each species is discussed in relation to their respective original habitats. Our study additionally provides evidence on the most resistant phytoplankton groups in a future warming scenario.
doi:10.1098/rspb.2011.0160
PMCID: PMC3189365  PMID: 21508031
phytoplankton; climate change; warming; genetic adaptation; ratchet technique
20.  Palaeoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II 
Two major geological problems regarding the origin of oxygenic photosynthesis are (i) identifying a source of oxygen pre-dating the biological oxygen production and capable of driving the evolution of oxygen tolerance, and (ii) determining when oxygenic photosynthesis evolved. One solution to the first problem is the accumulation of photochemically produced H2O2 at the surface of the glaciers and its subsequent incorporation into ice. Melting at the glacier base would release H2O2, which interacts with seawater to produce O2 in an environment shielded from the lethal levels of ultraviolet radiation needed to produce H2O2. Answers to the second problem are controversial and range from 3.8 to 2.2 Gyr ago. A sceptical view, based on the metals that have the redox potentials close to oxygen, argues for the late end of the range. The preponderance of geological evidence suggests little or no oxygen in the Late Archaean atmosphere (less than 1 ppm). The main piece of evidence for an earlier evolution of oxygenic photosynthesis comes from lipid biomarkers. Recent work, however, has shown that 2-methylhopanes, once thought to be unique biomarkers for cyanobacteria, are also produced anaerobically in significant quantities by at least two strains of anoxygenic phototrophs. Sterane biomarkers provide the strongest evidence for a date 2.7 Gyr ago or above, and could also be explained by the common evolutionary pattern of replacing anaerobic enzymes with oxygen-dependent ones. Although no anaerobic sterol synthesis pathway has been identified in the modern biosphere, enzymes that perform the necessary chemistry do exist. This analysis suggests that oxygenic photosynthesis could have evolved close in geological time to the Makganyene Snowball Earth Event and argues for a causal link between the two.
doi:10.1098/rstb.2008.0024
PMCID: PMC2606766  PMID: 18487128
Great Oxygenation Event; sterol biosynthesis; Makganyene Snowball Earth
21.  Reconnecting to the Biosphere 
Ambio  2011;40(7):719-738.
Humanity has emerged as a major force in the operation of the biosphere, with a significant imprint on the Earth System, challenging social–ecological resilience. This new situation calls for a fundamental shift in perspectives, world views, and institutions. Human development and progress must be reconnected to the capacity of the biosphere and essential ecosystem services to be sustained. Governance challenges include a highly interconnected and faster world, cascading social–ecological interactions and planetary boundaries that create vulnerabilities but also opportunities for social–ecological change and transformation. Tipping points and thresholds highlight the importance of understanding and managing resilience. New modes of flexible governance are emerging. A central challenge is to reconnect these efforts to the changing preconditions for societal development as active stewards of the Earth System. We suggest that the Millennium Development Goals need to be reframed in such a planetary stewardship context combined with a call for a new social contract on global sustainability. The ongoing mind shift in human relations with Earth and its boundaries provides exciting opportunities for societal development in collaboration with the biosphere—a global sustainability agenda for humanity.
doi:10.1007/s13280-011-0184-y
PMCID: PMC3357749  PMID: 22338712
Social–ecological systems; Resilience; Ecosystem services; Natural capital; Adaptive governance; Planetary stewardship
22.  Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms: an introduction 
Environmental constraints in aquatic habitats have become topics of concern to both the scientific community and the public at large. In particular, coastal and freshwater habitats are subject to dramatic variability in various environmental factors, as a result of both natural and anthropogenic processes. The protection and sustainable management of all aquatic habitats requires greater understanding of how environmental constraints influence aquatic organisms. Locomotion and predator–prey interactions are intimately linked and fundamental to the survival of mobile aquatic organisms. This paper summarizes the main points from the review and research articles which comprise the theme issue ‘Environmental constraints upon locomotion and predator–prey interactions in aquatic organisms’. The articles explore how natural and anthropogenic factors can constrain these two fundamental activities in a diverse range of organisms from phytoplankton to marine mammals. Some major environmental constraints derive from the intrinsic properties of the fluid and are mechanical in nature, such as viscosity and flow regime. Other constraints derive from direct effects of factors, such as temperature, oxygen content of the water or turbidity, upon the mechanisms underlying the performance of locomotion and predator–prey interactions. The effect of these factors on performance at the tissue and organ level is reflected in constraints upon performance of the whole organism. All these constraints can influence behaviour. Ultimately, they can have an impact on ecological performance. One issue that requires particular attention is how factors such as temperature and oxygen can exert different constraints on the physiology and behaviour of different taxa and the ecological implications of this. Given the multiplicity of constraints, the complexity of their interactions, and the variety of biological levels at which they can act, there is a clear need for integration between the fields of physiology, biomechanics, behaviour, ecology, biological modelling and evolution in both laboratory and field studies. For studies on animals in their natural environment, further technological advances are required to allow investigation of how the prevailing physico-chemical conditions influence basic physiological processes and behaviour.
doi:10.1098/rstb.2007.2078
PMCID: PMC2042526  PMID: 17472928
locomotion; predator–prey interactions; temperature; oxygen; turbidity; aquatic organisms
23.  Immunomodulation by Different Types of N-Oxides in the Hemocytes of the Marine Bivalve Mytilus galloprovincialis 
PLoS ONE  2012;7(5):e36937.
The potential toxicity of engineered nanoparticles (NPs) for humans and the environment represents an emerging issue. Since the aquatic environment represents the ultimate sink for NP deposition, the development of suitable assays is needed to evaluate the potential impact of NPs on aquatic biota. The immune system is a sensitive target for NPs, and conservation of innate immunity represents an useful basis for studying common biological responses to NPs. Suspension-feeding invertebrates, such as bivalves, are particularly at risk to NP exposure, since they have extremely developed systems for uptake of nano and microscale particles integral to intracellular digestion and cellular immunity. Evaluation of the effects of NPs on functional parameters of bivalve immunocytes, the hemocytes, may help understanding the major toxic mechanisms and modes of actions that could be relevant for different NP types in aquatic organisms.In this work, a battery of assays was applied to the hemocytes of the marine bivalve Mytilus galloprovincialis to compare the in vitro effects of different n-oxides (n-TiO2, n-SiO2, n-ZnO, n-CeO2) chosen on the basis of their commercial and environmental relevance. Physico-chemical characterization of both primary particles and NP suspensions in artificial sea water-ASW was performed. Hemocyte lysosomal and mitochondrial parameters, oxyradical and nitric oxide production, phagocytic activity, as well as NP uptake, were evaluated. The results show that different n-oxides rapidly elicited differential responses hemocytes in relation to their chemical properties, concentration, behavior in sea water, and interactions with subcellular compartments. These represent the most extensive data so far available on the effects of NPs in the cells of aquatic organisms. The results indicate that Mytilus hemocytes can be utilized as a suitable model for screening the potential effects of NPs in the cells of aquatic invertebrates, and may provide a basis for future experimental work for designing environmentally safer nanomaterials.
doi:10.1371/journal.pone.0036937
PMCID: PMC3350491  PMID: 22606310
24.  The Relationship of Previous Training and Experience of Journal Peer Reviewers to Subsequent Review Quality 
PLoS Medicine  2007;4(1):e40.
Background
Peer review is considered crucial to the selection and publication of quality science, but very little is known about the previous experiences and training that might identify high-quality peer reviewers. The reviewer selection processes of most journals, and thus the qualifications of their reviewers, are ill defined. More objective selection of peer reviewers might improve the journal peer review process and thus the quality of published science.
Methods and Findings
306 experienced reviewers (71% of all those associated with a specialty journal) completed a survey of past training and experiences postulated to improve peer review skills. Reviewers performed 2,856 reviews of 1,484 separate manuscripts during a four-year study period, all prospectively rated on a standardized quality scale by editors. Multivariable analysis revealed that most variables, including academic rank, formal training in critical appraisal or statistics, or status as principal investigator of a grant, failed to predict performance of higher-quality reviews. The only significant predictors of quality were working in a university-operated hospital versus other teaching environment and relative youth (under ten years of experience after finishing training). Being on an editorial board and doing formal grant (study section) review were each predictors for only one of our two comparisons. However, the predictive power of all variables was weak.
Conclusions
Our study confirms that there are no easily identifiable types of formal training or experience that predict reviewer performance. Skill in scientific peer review may be as ill defined and hard to impart as is “common sense.” Without a better understanding of those skills, it seems unlikely journals and editors will be successful in systematically improving their selection of reviewers. This inability to predict performance makes it imperative that all but the smallest journals implement routine review ratings systems to routinely monitor the quality of their reviews (and thus the quality of the science they publish).
A survey of experienced reviewers, asked about training they had received in peer review, found there are no easily identifiable types of formal training and experience that predict reviewer performance.
Editors' Summary
Background.
When medical researchers have concluded their research and written it up, the next step is to get it published as an article in a journal, so that the findings can be circulated widely. These published findings help determine subsequent research and clinical use. The editors of reputable journals, including PLoS Medicine, have to decide whether the articles sent to them are of good quality and accurate and whether they will be of interest to the readers of their journal. To do this they need to obtain specialist advice, so they contact experts in the topic of the research article and ask them to write reports. This is the process of scientific peer review, and the experts who write such reports are known as “peer reviewers.” Although the editors make the final decision, the advice and criticism of these peer reviewers to the editors is essential in making decisions on publication, and usually in requiring authors to make changes to their manuscript. The contribution that peer reviewers have made to the article by the time it is finally published may, therefore, be quite considerable.
Although peer review is accepted as a key part of the process for the publishing of medical research, many people have argued that there are flaws in the system. For example, there may be an element of luck involved; one author might find their paper being reviewed by a reviewer who is biased against the approach they have adopted or who is a very critical person by nature, and another author may have the good fortune to have their work considered by someone who is much more favorably disposed toward their work. Some reviewers are more knowledgeable and thorough in their work than others. The editors of medical journals try to take in account such biases and quality factors in their choice of peer reviewers or when assessing the reviews. Some journals have run training courses for experts who review for them regularly to try to make the standard of peer review as high as possible.
Why Was This Study Done?
It is hard for journal editors to know who will make a good peer reviewer, and there is no proven system for choosing them. The authors of this study wanted to identify the previous experiences and training that make up the background of good peer reviewers and compare them with the quality of the reviews provided. This would help journal editors select good people for the task in future, and as a result will affect the quality of science they publish for readers, including other researchers.
What Did the Researchers Do and Find?
The authors contacted all the regular reviewers from one specialist journal (Annals of Emergency Medicine). A total of 306 of these experienced reviewers (71% of all those associated with the journal) completed a survey of past training and experiences that might be expected to improve peer review skills. These reviewers had done 2,856 reviews of 1,484 separate manuscripts during a four-year study period, and during this time the quality of the reviews had been rated by the journal's editors. Surprisingly, most variables, including academic rank, formal training in critical appraisal or statistics, or status as principal investigator of a grant, failed to predict performance of higher-quality reviews. The only significant predictors of quality were working in a university-operated hospital versus other teaching environment and relative youth (under ten years of experience after finishing training), and even these were only weak predictors.
What Do These Findings Mean?
This study suggest that there are no easily identifiable types of formal training or experience that predict peer reviewer performance, although it is clear that some reviewers (and reviews) are better than others. The authors suggest that it is essential therefore that journals routinely monitor the quality of reviews submitted to them to ensure they are getting good advice (a practice that is not universal).
Additional Information.
Please access these Web sites via the online version of this summary at http://dx.doi.org/doi:10.1371/journal.pmed.0040040
• WAME is an association of editors from many countries who seek to foster international cooperation among editors of peer-reviewed medical journals
• The Fifth International Congress on Peer Review and Biomedical Publication is one of a series of conferences on peer review
• The PLoS Medicine guidelines for reviewers outline what we look for in a review
• The Council of Science Editors promotes ethical scientific publishing practices
• An editorial also published in this issue of PLoS Medicine discusses the peer review process further
doi:10.1371/journal.pmed.0040040
PMCID: PMC1796627  PMID: 17411314
25.  The Usefulness of Peer Review for Selecting Manuscripts for Publication: A Utility Analysis Taking as an Example a High-Impact Journal 
PLoS ONE  2010;5(6):e11344.
Background
High predictive validity – that is, a strong association between the outcome of peer review (usually, reviewers' ratings) and the scientific quality of a manuscript submitted to a journal (measured as citations of the later published paper) – does not as a rule suffice to demonstrate the usefulness of peer review for the selection of manuscripts. To assess usefulness, it is important to include in addition the base rate (proportion of submissions that are fundamentally suitable for publication) and the selection rate (the proportion of submissions accepted).
Methodology/Principal Findings
Taking the example of the high-impact journal Angewandte Chemie International Edition (AC-IE), we present a general approach for determining the usefulness of peer reviews for the selection of manuscripts for publication. The results of our study show that peer review is useful: 78% of the submissions accepted by AC-IE are correctly accepted for publication when the editor's decision is based on one review, 69% of the submissions are correctly accepted for publication when the editor's decision is based on two reviews, and 65% of the submissions are correctly accepted for publication when the editor's decision is based on three reviews.
Conclusions/Significance
The paper points out through what changes in the selection rate, base rate or validity coefficient a higher success rate (utility) in the AC-IE selection process could be achieved.
doi:10.1371/journal.pone.0011344
PMCID: PMC2893207  PMID: 20596540

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