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1.  Fungal Diversity in Deep-Sea Hydrothermal Ecosystems▿ †  
Applied and Environmental Microbiology  2009;75(20):6415-6421.
Deep-sea hydrothermal ecosystems are considered oases of life in oceans. Since the discovery of these ecosystems in the late 1970s, many endemic species of Bacteria, Archaea, and other organisms, such as annelids and crabs, have been described. Considerable knowledge has been acquired about the diversity of (micro)organisms in these ecosystems, but the diversity of fungi has not been studied to date. These organisms are considered key organisms in terrestrial ecosystems because of their ecological functions and especially their ability to degrade organic matter. The lack of knowledge about them in the sea reflects the widely held belief that fungi are terrestrial organisms. The first inventory of such organisms in deep-sea hydrothermal environments was obtained in this study. Fungal diversity was investigated by analyzing the small-subunit rRNA gene sequences amplified by culture-independent PCR using DNA extracts from hydrothermal samples and from a culture collection that was established. Our work revealed an unsuspected diversity of species in three of the five fungal phyla. We found a new branch of Chytridiomycota forming an ancient evolutionary lineage. Many of the species identified are unknown, even at higher taxonomic levels in the Chytridiomycota, Ascomycota, and Basidiomycota. This work opens the way to new studies of the diversity, ecology, and physiology of fungi in oceans and might stimulate new prospecting for biomolecules. From an evolutionary point of view, the diversification of fungi in the oceans can no longer be ignored.
PMCID: PMC2765129  PMID: 19633124
2.  Low endemism, continued deep-shallow interchanges, and evidence for cosmopolitan distributions in free-living marine nematodes (order Enoplida) 
Nematodes represent the most abundant benthic metazoa in one of the largest habitats on earth, the deep sea. Characterizing major patterns of biodiversity within this dominant group is a critical step towards understanding evolutionary patterns across this vast ecosystem. The present study has aimed to place deep-sea nematode species into a phylogenetic framework, investigate relationships between shallow water and deep-sea taxa, and elucidate phylogeographic patterns amongst the deep-sea fauna.
Molecular data (18 S and 28 S rRNA) confirms a high diversity amongst deep-sea Enoplids. There is no evidence for endemic deep-sea lineages in Maximum Likelihood or Bayesian phylogenies, and Enoplids do not cluster according to depth or geographic location. Tree topologies suggest frequent interchanges between deep-sea and shallow water habitats, as well as a mixture of early radiations and more recently derived lineages amongst deep-sea taxa. This study also provides convincing evidence of cosmopolitan marine species, recovering a subset of Oncholaimid nematodes with identical gene sequences (18 S, 28 S and cox1) at trans-Atlantic sample sites.
The complex clade structures recovered within the Enoplida support a high global species richness for marine nematodes, with phylogeographic patterns suggesting the existence of closely related, globally distributed species complexes in the deep sea. True cosmopolitan species may additionally exist within this group, potentially driven by specific life history traits of Enoplids. Although this investigation aimed to intensively sample nematodes from the order Enoplida, specimens were only identified down to genus (at best) and our sampling regime focused on an infinitesimal small fraction of the deep-sea floor. Future nematode studies should incorporate an extended sample set covering a wide depth range (shelf, bathyal, and abyssal sites), utilize additional genetic loci (e.g. mtDNA) that are informative at the species level, and apply high-throughput sequencing methods to fully assay community diversity. Finally, further molecular studies are needed to determine whether phylogeographic patterns observed in Enoplids are common across other ubiquitous marine groups (e.g. Chromadorida, Monhysterida).
PMCID: PMC3022606  PMID: 21167065
3.  Diversity of Meiofauna from the 9°50′N East Pacific Rise across a Gradient of Hydrothermal Fluid Emissions 
PLoS ONE  2010;5(8):e12321.
We studied the meiofauna community at deep-sea hydrothermal vents along a gradient of vent fluid emissions in the axial summit trought (AST) of the East Pacific Rise 9°50′N region. The gradient ranged from extreme high temperatures, high sulfide concentrations, and low pH at sulfide chimneys to ambient deep-sea water conditions on bare basalt. We explore meiofauna diversity and abundance, and discuss its possible underlying ecological and evolutionary processes.
Methodology/Principal Findings
After sampling in five physico-chemically different habitats, the meiofauna was sorted, counted and classified. Abundances were low at all sites. A total of 52 species were identified at vent habitats. The vent community was dominated by hard substrate generalists that also lived on bare basalt at ambient deep-sea temperature in the axial summit trough (AST generalists). Some vent species were restricted to a specific vent habitat (vent specialists), but others occurred over a wide range of physico-chemical conditions (vent generalists). Additionally, 35 species were only found on cold bare basalt (basalt specialists). At vent sites, species richness and diversity clearly increased with decreasing influence of vent fluid emissions from extreme flow sulfide chimney (no fauna), high flow pompei worm (S: 4–7, H'loge: 0.11–0.45), vigorous flow tubeworm (S: 8–23; H'loge: 0.44–2.00) to low flow mussel habitats (S: 28–31; H'loge: 2.34–2.60).
Our data suggest that with increasing temperature and toxic hydrogen sulfide concentrations and increasing amplitude of variation of these factors, fewer species are able to cope with these extreme conditions. This results in less diverse communities in more extreme habitats. The finding of many species being present at sites with and without vent fluid emissions points to a non endemic deep-sea hydrothermal vent meiofaunal community. This is in contrast to a mostly endemic macrofauna but similar to what is known for meiofauna from shallow-water vents.
PMCID: PMC2938375  PMID: 20856898
4.  Importance of Saprotrophic Freshwater Fungi for Pollen Degradation 
PLoS ONE  2014;9(4):e94643.
Fungi and bacteria are the major organic matter (OM) decomposers in aquatic ecosystems. While bacteria are regarded as primary mineralizers in the pelagic zone of lakes and oceans, fungi dominate OM decomposition in streams and wetlands. Recent findings indicate that fungal communities are also active in lakes, but little is known about their diversity and interactions with bacteria. Therefore, the decomposer niche overlap of saprotrophic fungi and bacteria was studied on pollen (as a seasonally recurring source of fine particulate OM) by performing microcosm experiments with three different lake types. Special emphasis was placed on analysis of fungal community composition and diversity. We hypothesized that (I) pollen select for small saprotrophic fungi and at the same time for typical particle-associated bacteria; (II) fungal communities form specific free-living and attached sub-communities in each lake type; (III) the ratio between fungi or bacteria on pollen is controlled by the lake's chemistry. Bacteria-to-fungi ratios were determined by quantitative PCR (qPCR), and bacterial and fungal diversity were studied by clone libraries and denaturing gradient gel electrophoresis (DGGE) fingerprints. A protease assay was used to identify functional differences between treatments. For generalization, systematic differences in bacteria-to-fungi ratios were analyzed with a dataset from the nearby Baltic Sea rivers. High abundances of Chytridiomycota as well as occurrences of Cryptomycota and yeast-like fungi confirm the decomposer niche overlap of saprotrophic fungi and bacteria on pollen. As hypothesized, microbial communities consistently differed between the lake types and exhibited functional differences. Bacteria-to-fungi ratios correlated well with parameters such as organic carbon and pH. The importance of dissolved organic carbon and nitrogen for bacteria-to-fungi ratios was supported by the Baltic Sea river dataset. Our findings highlight the fact that carbon-to-nitrogen ratios may also control fungal contributions to OM decomposition in aquatic ecosystems.
PMCID: PMC3986395  PMID: 24732324
5.  Ancient Origin of the Modern Deep-Sea Fauna 
PLoS ONE  2012;7(10):e46913.
The origin and possible antiquity of the spectacularly diverse modern deep-sea fauna has been debated since the beginning of deep-sea research in the mid-nineteenth century. Recent hypotheses, based on biogeographic patterns and molecular clock estimates, support a latest Mesozoic or early Cenozoic date for the origin of key groups of the present deep-sea fauna (echinoids, octopods). This relatively young age is consistent with hypotheses that argue for extensive extinction during Jurassic and Cretaceous Oceanic Anoxic Events (OAEs) and the mid-Cenozoic cooling of deep-water masses, implying repeated re-colonization by immigration of taxa from shallow-water habitats. Here we report on a well-preserved echinoderm assemblage from deep-sea (1000–1500 m paleodepth) sediments of the NE-Atlantic of Early Cretaceous age (114 Ma). The assemblage is strikingly similar to that of extant bathyal echinoderm communities in composition, including families and genera found exclusively in modern deep-sea habitats. A number of taxa found in the assemblage have no fossil record at shelf depths postdating the assemblage, which precludes the possibility of deep-sea recolonization from shallow habitats following episodic extinction at least for those groups. Our discovery provides the first key fossil evidence that a significant part of the modern deep-sea fauna is considerably older than previously assumed. As a consequence, most major paleoceanographic events had far less impact on the diversity of deep-sea faunas than has been implied. It also suggests that deep-sea biota are more resilient to extinction events than shallow-water forms, and that the unusual deep-sea environment, indeed, provides evolutionary stability which is very rarely punctuated on macroevolutionary time scales.
PMCID: PMC3468611  PMID: 23071660
6.  Deep-Sea Biodiversity in the Mediterranean Sea: The Known, the Unknown, and the Unknowable 
PLoS ONE  2010;5(8):e11832.
Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.
PMCID: PMC2914020  PMID: 20689848
7.  Ecology and Biogeography of Free-Living Nematodes Associated with Chemosynthetic Environments in the Deep Sea: A Review 
PLoS ONE  2010;5(8):e12449.
Here, insight is provided into the present knowledge on free-living nematodes associated with chemosynthetic environments in the deep sea. It was investigated if the same trends of high standing stock, low diversity, and the dominance of a specialized fauna, as observed for macro-invertebrates, are also present in the nematodes in both vents and seeps.
This review is based on existing literature, in combination with integrated analysis of datasets, obtained through the Census of Marine Life program on Biogeography of Deep-Water Chemosynthetic Ecosystems (ChEss).
Nematodes are often thriving in the sulphidic sediments of deep cold seeps, with standing stock values ocassionaly exceeding largely the numbers at background sites. Vents seem not characterized by elevated densities. Both chemosynthetic driven ecosystems are showing low nematode diversity, and high dominance of single species. Genera richness seems inversely correlated to vent and seep fluid emissions, associated with distinct habitat types. Deep-sea cold seeps and hydrothermal vents are, however, highly dissimilar in terms of community composition and dominant taxa. There is no unique affinity of particular nematode taxa with seeps or vents.
It seems that shallow water relatives, rather than typical deep-sea taxa, have successfully colonized the reduced sediments of seeps at large water depth. For vents, the taxonomic similarity with adjacent regular sediments is much higher, supporting rather the importance of local adaptation, than that of long distance distribution. Likely the ephemeral nature of vents, its long distance offshore and the absence of pelagic transport mechanisms, have prevented so far the establishment of a successful and typical vent nematode fauna. Some future perspectives in meiofauna research are provided in order to get a more integrated picture of vent and seep biological processes, including all components of the marine ecosystem.
PMCID: PMC2929199  PMID: 20805986
8.  Comparative metagenomics of bathypelagic plankton and bottom sediment from the Sea of Marmara 
The ISME journal  2010;5(2):285-304.
To extend comparative metagenomic analyses of the deep-sea, we produced metagenomic data by direct 454 pyrosequencing from bathypelagic plankton (1000 m depth) and bottom sediment of the Sea of Marmara, the gateway between the Eastern Mediterranean and the Black Seas. Data from small subunit ribosomal RNA (SSU rRNA) gene libraries and direct pyrosequencing of the same samples indicated that Gamma- and Alpha-proteobacteria, followed by Bacteroidetes, dominated the bacterial fraction in Marmara deep-sea plankton, whereas Planctomycetes, Delta- and Gamma-proteobacteria were the most abundant groups in high bacterial-diversity sediment. Group I Crenarchaeota/Thaumarchaeota dominated the archaeal plankton fraction, although group II and III Euryarchaeota were also present. Eukaryotes were highly diverse in SSU rRNA gene libraries, with group I (Duboscquellida) and II (Syndiniales) alveolates and Radiozoa dominating plankton, and Opisthokonta and Alveolates, sediment. However, eukaryotic sequences were scarce in pyrosequence data. Archaeal amo genes were abundant in plankton, suggesting that Marmara planktonic Thaumarchaeota are ammonia oxidizers. Genes involved in sulfate reduction, carbon monoxide oxidation, anammox and sulfatases were over-represented in sediment. Genome recruitment analyses showed that Alteromonas macleodii ‘surface ecotype', Pelagibacter ubique and Nitrosopumilus maritimus were highly represented in 1000 m-deep plankton. A comparative analysis of Marmara metagenomes with ALOHA deep-sea and surface plankton, whale carcasses, Peru subsurface sediment and soil metagenomes clustered deep-sea Marmara plankton with deep-ALOHA plankton and whale carcasses, likely because of the suboxic conditions in the deep Marmara water column. The Marmara sediment clustered with the soil metagenome, highlighting the common ecological role of both types of microbial communities in the degradation of organic matter and the completion of biogeochemical cycles.
PMCID: PMC3105693  PMID: 20668488
deep-sea; anaerobic respiration; carbon fixation; carbon cycle; sulfate reduction; ammonia oxidation
9.  Phylogenetic Diversity of Nitrogenase (nifH) Genes in Deep-Sea and Hydrothermal Vent Environments of the Juan de Fuca Ridge 
The subseafloor microbial habitat associated with typical unsedimented mid-ocean-ridge hydrothermal vent ecosystems may be limited by the availability of fixed nitrogen, inferred by the low ammonium and nitrate concentrations measured in diffuse hydrothermal fluid. Dissolved N2 gas, the largest reservoir of nitrogen in the ocean, is abundant in deep-sea and hydrothermal vent fluid. In order to test the hypothesis that biological nitrogen fixation plays an important role in nitrogen cycling in the subseafloor associated with unsedimented hydrothermal vents, degenerate PCR primers were designed to amplify the nitrogenase iron protein gene nifH from hydrothermal vent fluid. A total of 120 nifH sequences were obtained from four samples: a nitrogen-poor diffuse vent named marker 33 on Axial Volcano, sampled twice over a period of 1 year as its temperature decreased; a nitrogen-rich diffuse vent near Puffer on Endeavour Segment; and deep seawater with no detectable hydrothermal plume signal. Subseafloor nifH genes from marker 33 and Puffer are related to anaerobic clostridia and sulfate reducers. Other nifH genes unique to the vent samples include proteobacteria and divergent Archaea. All of the nifH genes from the deep-seawater sample are most closely related to the thermophilic, anaerobic archaeon Methanococcus thermolithotrophicus (77 to 83% amino acid similarity). These results provide the first genetic evidence of potential nitrogen fixers in hydrothermal vent environments and indicate that at least two sources contribute to the diverse assemblage of nifH genes detected in hydrothermal vent fluid: nifH genes from an anaerobic, hot subseafloor and nifH genes from cold, oxygenated deep seawater.
PMCID: PMC143675  PMID: 12571018
10.  Growth and Phylogenetic Properties of Novel Bacteria Belonging to the Epsilon Subdivision of the Proteobacteria Enriched from Alvinella pompejana and Deep-Sea Hydrothermal Vents 
Applied and Environmental Microbiology  2001;67(10):4566-4572.
Recent molecular characterizations of microbial communities from deep-sea hydrothermal sites indicate the predominance of bacteria belonging to the epsilon subdivision of Proteobacteria (epsilon Proteobacteria). Here, we report the first enrichments and characterizations of four epsilon Proteobacteria that are directly associated with Alvinella pompejana, a deep sea hydrothermal vent polychete, or with hydrothermal vent chimney samples. These novel bacteria were moderately thermophilic sulfur-reducing heterotrophs growing on formate as the energy and carbon source. In addition, two of them (Am-H and Ex-18.2) could grow on sulfur lithoautrotrophically using hydrogen as the electron donor. Optimal growth temperatures of the bacteria ranged from 41 to 45°C. Phylogenetic analysis of the small-subunit ribosomal gene of the two heterotrophic bacteria demonstrated 95% similarity to Sulfurospirillum arcachonense, an epsilon Proteobacteria isolated from an oxidized marine surface sediment. The autotrophic bacteria grouped within a deeply branching clade of the epsilon Proteobacteria, to date composed only of uncultured bacteria detected in a sample from a hydrothermal vent along the mid-Atlantic ridge. A molecular survey of various hydrothermal vent environments demonstrated the presence of two of these bacteria (Am-N and Am-H) in more than one geographic location and habitat. These results suggest that certain epsilon Proteobacteria likely fill important niches in the environmental habitats of deep-sea hydrothermal vents, where they contribute to overall carbon and sulfur cycling at moderate thermophilic temperatures.
PMCID: PMC93204  PMID: 11571157
11.  Integrated Metagenomic and Metatranscriptomic Analyses of Microbial Communities in the Meso- and Bathypelagic Realm of North Pacific Ocean 
Marine Drugs  2013;11(10):3777-3801.
Although emerging evidence indicates that deep-sea water contains an untapped reservoir of high metabolic and genetic diversity, this realm has not been studied well compared with surface sea water. The study provided the first integrated meta-genomic and -transcriptomic analysis of the microbial communities in deep-sea water of North Pacific Ocean. DNA/RNA amplifications and simultaneous metagenomic and metatranscriptomic analyses were employed to discover information concerning deep-sea microbial communities from four different deep-sea sites ranging from the mesopelagic to pelagic ocean. Within the prokaryotic community, bacteria is absolutely dominant (~90%) over archaea in both metagenomic and metatranscriptomic data pools. The emergence of archaeal phyla Crenarchaeota, Euryarchaeota, Thaumarchaeota, bacterial phyla Actinobacteria, Firmicutes, sub-phyla Betaproteobacteria, Deltaproteobacteria, and Gammaproteobacteria, and the decrease of bacterial phyla Bacteroidetes and Alphaproteobacteria are the main composition changes of prokaryotic communities in the deep-sea water, when compared with the reference Global Ocean Sampling Expedition (GOS) surface water. Photosynthetic Cyanobacteria exist in all four metagenomic libraries and two metatranscriptomic libraries. In Eukaryota community, decreased abundance of fungi and algae in deep sea was observed. RNA/DNA ratio was employed as an index to show metabolic activity strength of microbes in deep sea. Functional analysis indicated that deep-sea microbes are leading a defensive lifestyle.
PMCID: PMC3826135  PMID: 24152557
deep-sea microbial community; metagenomics; metatranscriptomics; strength of metabolic activity
12.  Do Larval Supply and Recruitment Vary among Chemosynthetic Environments of the Deep Sea? 
PLoS ONE  2010;5(7):e11646.
The biological communities that inhabit chemosynthetic environments exist in an ephemeral and patchily distributed habitat with unique physicochemical properties that lead to high endemicity. Consequently, the maintenance and recovery from perturbation of the populations in these habitats is, arguably, mainly regulated by larval supply and recruitment.
Methodology/Principal Findings
We use data from the published scientific literature to: (1) compare the magnitudes of and variability in larval supply and settlement and recruitment at hydrothermal vents, seeps, and whale, wood and kelp falls; (2) explore factors that affect these life history processes, when information is available; and (3) explore taxonomic affinities in the recruit assemblages of the different chemosynthetic habitats, using multivariate statistical techniques. Larval supply at vents can vary across segments by several orders of magnitude for gastropods; for bivalves, supply is similar at vents on different segments, and at cold seeps. The limited information on larval development suggests that dispersal potential may be highest for molluscs from cold seeps, intermediate for siboglinids at vents and lowest for the whale-bone siboglinid Osedax. Settlement is poorly studied and only at vents and seeps, but tends to be highest near an active source of emanating fluid in both habitats. Rate of recruitment at vents is more variable among studies within a segment than among segments. Across different chemosynthetic habitats, recruitment rate of bivalves is much more variable than that of gastropods and polychaetes. Total recruitment rate ranges only between 0.1 and 1 ind dm−2 d−1 across all chemosynthetic habitats, falling above rates in the non-reducing deep sea. The recruit assemblages at vents, seeps and kelp falls have lower taxonomic breadth, and include more families and genera that have many species more closely related to each other than those at whale and wood falls. Vents also have the most uneven taxonomic structure, with fewer recruits represented by higher taxonomic levels (phyla, orders, classes) compared to seeps and wood and kelp falls, whereas the opposite is true at whale falls.
Based on our evaluation of the literature, the patterns and regulatory factors of the early history processes in chemosynthetic environments in the deep sea remain poorly understood. More research focused on these early life history stages will allow us to make inferences about the ecological and biogeographic linkages among the reducing habitats in the deep sea.
PMCID: PMC2906503  PMID: 20657831
13.  Advances in Taxonomy, Ecology, and Biogeography of Dirivultidae (Copepoda) Associated with Chemosynthetic Environments in the Deep Sea 
PLoS ONE  2010;5(8):e9801.
Copepoda is one of the most prominent higher taxa with almost 80 described species at deep-sea hydrothermal vents. The unique copepod family Dirivultidae with currently 50 described species is the most species rich invertebrate family at hydrothermal vents.
Methodology/Principal Findings
We reviewed the literature of Dirivultidae and provide a complete key to species, and map geographical and habitat specific distribution. In addition we discuss the ecology and origin of this family.
Dirivultidae are only present at deep-sea hydrothermal vents and along the axial summit trough of midocean ridges, with the exception of Dirivultus dentaneus found associated with Lamellibrachia species at 1125 m depth off southern California. To our current knowledge Dirivultidae are unknown from shallow-water vents, seeps, whale falls, and wood falls. They are a prominent part of all communities at vents and in certain habitat types (like sulfide chimneys colonized by pompei worms) they are the most abundant animals. They are free-living on hard substrate, mostly found in aggregations of various foundation species (e.g. alvinellids, vestimentiferans, and bivalves). Most dirivultid species colonize more than one habitat type. Dirivultids have a world-wide distribution, but most genera and species are endemic to a single biogeographic region. Their origin is unclear yet, but immigration from other deep-sea chemosynthetic habitats (stepping stone hypothesis) or from the deep-sea sediments seems unlikely, since Dirivultidae are unknown from these environments. Dirivultidae is the most species rich family and thus can be considered the most successful taxon at deep-sea vents.
PMCID: PMC2868908  PMID: 20838422
14.  Biogeography of Persephonella in deep-sea hydrothermal vents of the Western Pacific 
Deep-sea hydrothermal vent fields are areas on the seafloor with high biological productivity fueled by microbial chemosynthesis. Members of the Aquificales genus Persephonella are obligately chemosynthetic bacteria, and appear to be key players in carbon, sulfur, and nitrogen cycles in high temperature habitats at deep-sea vents. Although this group of bacteria has cosmopolitan distribution in deep-sea hydrothermal ecosystem around the world, little is known about their population structure such as intraspecific genomic diversity, distribution pattern, and phenotypic diversity. We developed the multi-locus sequence analysis (MLSA) scheme for their genomic characterization. Sequence variation was determined in five housekeeping genes and one functional gene of 36 Persephonella hydrogeniphila strains originated from the Okinawa Trough and the South Mariana Trough (SNT). Although the strains share >98.7% similarities in 16S rRNA gene sequences, MLSA revealed 35 different sequence types (ST), indicating their extensive genomic diversity. A phylogenetic tree inferred from all concatenated gene sequences revealed the clustering of isolates according to the geographic origin. In addition, the phenotypic clustering pattern inferred from whole-cell matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF/MS) analysis can be correlated to their MLSA clustering pattern. This study represents the first MLSA combined with phenotypic analysis indicative of allopatric speciation of deep-sea hydrothermal vent bacteria.
PMCID: PMC3635849  PMID: 23630523
population structure; biogeography; deep-sea hydrothermal vent; Persephonella; Aquificales; MLSA; MALDI-TOF/MS; chemolithoautotroph
15.  Archaea in Yellowstone Lake 
The ISME Journal  2011;5(11):1784-1795.
The Yellowstone geothermal complex has yielded foundational discoveries that have significantly enhanced our understanding of the Archaea. This study continues on this theme, examining Yellowstone Lake and its lake floor hydrothermal vents. Significant Archaea novelty and diversity were found associated with two near-surface photic zone environments and two vents that varied in their depth, temperature and geochemical profile. Phylogenetic diversity was assessed using 454-FLX sequencing (∼51 000 pyrosequencing reads; V1 and V2 regions) and Sanger sequencing of 200 near-full-length polymerase chain reaction (PCR) clones. Automated classifiers (Ribosomal Database Project (RDP) and Greengenes) were problematic for the 454-FLX reads (wrong domain or phylum), although BLAST analysis of the 454-FLX reads against the phylogenetically placed full-length Sanger sequenced PCR clones proved reliable. Most of the archaeal diversity was associated with vents, and as expected there were differences between the vents and the near-surface photic zone samples. Thaumarchaeota dominated all samples: vent-associated organisms corresponded to the largely uncharacterized Marine Group I, and in surface waters, ∼69–84% of the 454-FLX reads matched archaeal clones representing organisms that are Nitrosopumilus maritimus-like (96–97% identity). Importance of the lake nitrogen cycling was also suggested by >5% of the alkaline vent phylotypes being closely related to the nitrifier Candidatus Nitrosocaldus yellowstonii. The Euryarchaeota were primarily related to the uncharacterized environmental clones that make up the Deep Sea Euryarchaeal Group or Deep Sea Hydrothermal Vent Group-6. The phylogenetic parallels of Yellowstone Lake archaea to marine microorganisms provide opportunities to examine interesting evolutionary tracks between freshwater and marine lineages.
PMCID: PMC3197168  PMID: 21544103
archaea; Yellowstone Lake; pyrosequencing; N cycling; spatial distribution
16.  Biodiversity of the Deep-Sea Continental Margin Bordering the Gulf of Maine (NW Atlantic): Relationships among Sub-Regions and to Shelf Systems 
PLoS ONE  2010;5(11):e13832.
In contrast to the well-studied continental shelf region of the Gulf of Maine, fundamental questions regarding the diversity, distribution, and abundance of species living in deep-sea habitats along the adjacent continental margin remain unanswered. Lack of such knowledge precludes a greater understanding of the Gulf of Maine ecosystem and limits development of alternatives for conservation and management.
Methodology/Principal Findings
We use data from the published literature, unpublished studies, museum records and online sources, to: (1) assess the current state of knowledge of species diversity in the deep-sea habitats adjacent to the Gulf of Maine (39–43°N, 63–71°W, 150–3000 m depth); (2) compare patterns of taxonomic diversity and distribution of megafaunal and macrofaunal species among six distinct sub-regions and to the continental shelf; and (3) estimate the amount of unknown diversity in the region. Known diversity for the deep-sea region is 1,671 species; most are narrowly distributed and known to occur within only one sub-region. The number of species varies by sub-region and is directly related to sampling effort occurring within each. Fishes, corals, decapod crustaceans, molluscs, and echinoderms are relatively well known, while most other taxonomic groups are poorly known. Taxonomic diversity decreases with increasing distance from the continental shelf and with changes in benthic topography. Low similarity in faunal composition suggests the deep-sea region harbours faunal communities distinct from those of the continental shelf. Non-parametric estimators of species richness suggest a minimum of 50% of the deep-sea species inventory remains to be discovered.
The current state of knowledge of biodiversity in this deep-sea region is rudimentary. Our ability to answer questions is hampered by a lack of sufficient data for many taxonomic groups, which is constrained by sampling biases, life-history characteristics of target species, and the lack of trained taxonomists.
PMCID: PMC2988790  PMID: 21124960
17.  Comparative Composition, Diversity and Trophic Ecology of Sediment Macrofauna at Vents, Seeps and Organic Falls 
PLoS ONE  2012;7(4):e33515.
Sediments associated with hydrothermal venting, methane seepage and large organic falls such as whale, wood and plant detritus create deep-sea networks of soft-sediment habitats fueled, at least in part, by the oxidation of reduced chemicals. Biological studies at deep-sea vents, seeps and organic falls have looked at macrofaunal taxa, but there has yet to be a systematic comparison of the community-level attributes of sediment macrobenthos in various reducing ecosystems. Here we review key similarities and differences in the sediment-dwelling assemblages of each system with the goals of (1) generating a predictive framework for the exploration and study of newly identified reducing habitats, and (2) identifying taxa and communities that overlap across ecosystems. We show that deep-sea seep, vent and organic-fall sediments are highly heterogeneous. They sustain different geochemical and microbial processes that are reflected in a complex mosaic of habitats inhabited by a mixture of specialist (heterotrophic and symbiont-associated) and background fauna. Community-level comparisons reveal that vent, seep and organic-fall macrofauna are very distinct in terms of composition at the family level, although they share many dominant taxa among these highly sulphidic habitats. Stress gradients are good predictors of macrofaunal diversity at some sites, but habitat heterogeneity and facilitation often modify community structure. The biogeochemical differences across ecosystems and within habitats result in wide differences in organic utilization (i.e., food sources) and in the prevalence of chemosynthesis-derived nutrition. In the Pacific, vents, seeps and organic-falls exhibit distinct macrofaunal assemblages at broad-scales contributing to ß diversity. This has important implications for the conservation of reducing ecosystems, which face growing threats from human activities.
PMCID: PMC3319539  PMID: 22496753
18.  The contrasted evolutionary fates of deep-sea chemosynthetic mussels (Bivalvia, Bathymodiolinae)a 
Ecology and Evolution  2013;3(14):4748-4766.
Bathymodiolinae are giant mussels that were discovered at hydrothermal vents and harboring chemosynthetic symbionts. Due to their close phylogenetic relationship with seep species and tiny mussels from organic substrates, it was hypothesized that they gradually evolved from shallow to deeper environments, and specialized in decaying organic remains, then in seeps, and finally colonized deep-sea vents. Here, we present a multigene phylogeny that reveals that most of the genera are polyphyletic and/or paraphyletic. The robustness of the phylogeny allows us to revise the genus-level classification. Organic remains are robustly supported as the ancestral habitat for Bathymodiolinae. However, rather than a single step toward colonization of vents and seeps, recurrent habitat shifts from organic substrates to vents and seeps occurred during evolution, and never the reverse. This new phylogenetic framework challenges the gradualist scenarios “from shallow to deep.” Mussels from organic remains tolerate a large range of ecological conditions and display a spectacular species diversity contrary to vent mussels, although such habitats are yet underexplored compared to vents and seeps. Overall, our data suggest that for deep-sea mussels, the high specialization to vent habitats provides ecological success in this harsh habitat but also brings the lineage to a kind of evolutionary dead end.
PMCID: PMC3867909  PMID: 24363902
Bathymodiolinae; chemosynthetic ecosystem; deep-sea; evolution
19.  Metagenetic community analysis of microbial eukaryotes illuminates biogeographic patterns in deep-sea and shallow water sediments 
Molecular Ecology  2011;21(5):1048-1059.
Microbial eukaryotes (nematodes, protists, fungi, etc., loosely referred to as meiofauna) are ubiquitous in marine sediments and likely play pivotal roles in maintaining ecosystem function. Although the deep-sea benthos represents one of the world’s largest habitats, we lack a firm understanding of the biodiversity and community interactions amongst meiobenthic organisms in this ecosystem. Within this vast environment key questions concerning the historical genetic structure of species remain a mystery, yet have profound implications for our understanding of global biodiversity and how we perceive and mitigate the impact of environmental change and anthropogenic disturbance. Using a metagenetic approach, we present an assessment of microbial eukaryote communities across depth (shallow water to abyssal) and ocean basins (deep-sea Pacific and Atlantic). Within the 12 sites examined, our results suggest that some taxa can maintain eurybathic ranges and cosmopolitan deep-sea distributions, but the majority of species appear to be regionally restricted. For OCTUs reporting wide distributions, there appears to be a taxonomic bias towards a small subset of taxa in most phyla; such bias may be driven by specific life history traits amongst these organisms. In addition, low genetic divergence between geographically disparate deep-sea sites suggests either a shorter coalescence time between deep-sea regions or slower rates of evolution across this vast oceanic ecosystem. While high-throughput studies allow for broad assessment of genetic patterns across microbial eukaryote communities, intragenomic variation in rRNA gene copies and the patchy coverage of reference databases currently present substantial challenges for robust taxonomic interpretations of eukaryotic datasets.
PMCID: PMC3261328  PMID: 21985648
microbial eukaryotes; meiofauna; deep-sea; cosmopolitan species; 18S rRNA; phylogeography; 454 sequencing
20.  Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea 
The deep sea is Earth's largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over 2 years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes' intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. marisprofundi targets the host's body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep-sea biosphere.
PMCID: PMC3918590  PMID: 24575084
deep-sea methane seeps; nematodes hosts; deep-sea microsporidia parasitism; muscle decomposition; basal fungi in the deep sea
21.  Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities 
Hydrothermal vents differ both in surface input and subsurface geochemistry. The effects of these differences on their microbial communities are not clear. Here, we investigated both alpha and beta diversity of diffuse flow-associated microbial communities emanating from vents at a basalt-based hydrothermal system along the East Pacific Rise (EPR) and a sediment-based hydrothermal system, Guaymas Basin. Both Bacteria and Archaea were targeted using high throughput 16S rRNA gene pyrosequencing analyses. A unique aspect of this study was the use of a universal set of 16S rRNA gene primers to characterize total and diffuse flow-specific microbial communities from varied deep-sea hydrothermal environments. Both surrounding seawater and diffuse flow water samples contained large numbers of Marine Group I (MGI) Thaumarchaea and Gammaproteobacteria taxa previously observed in deep-sea systems. However, these taxa were geographically distinct and segregated according to type of spreading center. Diffuse flow microbial community profiles were highly differentiated. In particular, EPR dominant diffuse flow taxa were most closely associated with chemolithoautotrophs, and off axis water was dominated by heterotrophic-related taxa, whereas the opposite was true for Guaymas Basin. The diversity and richness of diffuse flow-specific microbial communities were strongly correlated to the relative abundance of Epsilonproteobacteria, proximity to macrofauna, and hydrothermal system type. Archaeal diversity was higher than or equivalent to bacterial diversity in about one third of the samples. Most diffuse flow-specific communities were dominated by OTUs associated with Epsilonproteobacteria, but many of the Guaymas Basin diffuse flow samples were dominated by either OTUs within the Planctomycetes or hyperthermophilic Archaea. This study emphasizes the unique microbial communities associated with geochemically and geographically distinct hydrothermal diffuse flow environments.
PMCID: PMC3721025  PMID: 23898323
diffuse flow; microbial diversity; 16S rRNA; pyrosequencing; hydrothermal vents
22.  Molecular Detection of Fungal Communities in the Hawaiian Marine Sponges Suberites zeteki and Mycale armata▿  
Applied and Environmental Microbiology  2008;74(19):6091-6101.
Symbiotic microbes play a variety of fundamental roles in the health and habitat ranges of their hosts. While prokaryotes in marine sponges have been broadly characterized, the diversity of sponge-inhabiting fungi has barely been explored using molecular approaches. Fungi are an important component of many marine and terrestrial ecosystems, and they may be an ecologically significant group in sponge-microbe interactions. This study tested the feasibility of using existing fungal primers for molecular analysis of sponge-associated fungal communities. None of the eight selected primer pairs yielded satisfactory results in fungal rRNA gene or internal transcribed spacer (ITS) clone library constructions. However, 3 of 10 denaturing gradient gel electrophoresis (DGGE) primer sets, which were designed to preferentially amplify fungal rRNA gene or ITS regions from terrestrial environmental samples, were successfully amplified from fungal targets in marine sponges. DGGE analysis indicated that fungal communities differ among different sponge species (Suberites zeteki and Mycale armata) and also vary between sponges and seawater. Sequence analysis of DGGE bands identified 23 and 21 fungal species from each of the two sponge species S. zeteki and M. armata, respectively. These species were representatives of 11 taxonomic orders and belonged to the phyla of Ascomycota (seven orders) and Basidiomycota (four orders). Five of these taxonomic orders (Malasseziales, Corticiales, Polyporales, Agaricales, and Dothideomycetes et Chaetothyriomcetes incertae sedis) have now been identified for the first time in marine sponges. Seven and six fungal species from S. zeteki and M. armata, respectively, are potentially new species because of their low sequence identity (≤98%) with their references in GenBank. Phylogenetic analysis indicated sponge-derived sequences were clustered into “marine fungus clades” with those from other marine habitats. This is the first report of molecular analysis of fungal communities in marine sponges, adding depth and dimension to our understanding of sponge-associated microbial communities.
PMCID: PMC2565983  PMID: 18676706
23.  The microbiology of deep-sea hydrothermal vent plumes: ecological and biogeographic linkages to seafloor and water column habitats 
Hydrothermal plumes are an important yet understudied component of deep-sea vent microbial ecosystems. The significance of plume microbial processes can be appreciated from three perspectives: (1) mediation of plume biogeochemistry, (2) dispersal of seafloor hydrothermal vent microbes between vents sites, (3) as natural laboratories for understanding the ecology, physiology, and function of microbial groups that are distributed throughout the pelagic deep sea. Plume microbiology has been largely neglected in recent years, especially relative to the extensive research conducted on seafloor and subseafloor systems. Rapidly advancing technologies for investigating microbial communities provide new motivation and opportunities to characterize this important microbial habitat. Here we briefly highlight microbial contributions to plume and broader ocean (bio)geochemistry and review recent work to illustrate the ecological and biogeographic linkages between plumes, seafloor vent habitats, and other marine habitats such as oxygen minimum zones (OMZs), cold seeps, and oil spills. 16S rRNA gene surveys and metagenomic/-transcriptomic data from plumes point to dominant microbial populations, genes, and functions that are also operative in OMZs (SUP05, ammonia-oxidizing Archaea, and SAR324 Deltaproteobacteria) and hydrocarbon-rich environments (methanotrophs). Plume microbial communities are distinct from those on the seafloor or in the subsurface but contain some signatures of these habitats, consistent with the notion that plumes are potential vectors for dispersal of microorganisms between seafloor vent sites. Finally, we put forward three pressing questions for the future of deep-sea hydrothermal plume research and consider interactions between vents and oceans on global scales.
PMCID: PMC3659317  PMID: 23720658
chemosynthesis; chemoautotroph; deep-sea; biogeochemistry; hydrothermal; vent; biogeography
24.  Detection of Putatively Thermophilic Anaerobic Methanotrophs in Diffuse Hydrothermal Vent Fluids 
The anaerobic oxidation of methane (AOM) is carried out by a globally distributed group of uncultivated Euryarchaeota, the anaerobic methanotrophic arachaea (ANME). In this work, we used G+C analysis of 16S rRNA genes to identify a putatively thermophilic ANME group and applied newly designed primers to study its distribution in low-temperature diffuse vent fluids from deep-sea hydrothermal vents. We found that the G+C content of the 16S rRNA genes (PGC) is significantly higher in the ANME-1GBa group than in other ANME groups. Based on the positive correlation between the PGC and optimal growth temperatures (Topt) of archaea, we hypothesize that the ANME-1GBa group is adapted to thrive at high temperatures. We designed specific 16S rRNA gene-targeted primers for the ANME-1 cluster to detect all phylogenetic groups within this cluster, including the deeply branching ANME-1GBa group. The primers were successfully tested both in silico and in experiments with sediment samples where ANME-1 phylotypes had previously been detected. The primers were further used to screen for the ANME-1 microorganisms in diffuse vent fluid samples from deep-sea hydrothermal vents in the Pacific Ocean, and sequences belonging to the ANME-1 cluster were detected in four individual vents. Phylotypes belonging to the ANME-1GBa group dominated in clone libraries from three of these vents. Our findings provide evidence of existence of a putatively extremely thermophilic group of methanotrophic archaea that occur in geographically and geologically distinct marine hydrothermal habitats.
PMCID: PMC3568577  PMID: 23183981
25.  Manganese(II)-Oxidizing Bacillus Spores in Guaymas Basin Hydrothermal Sediments and Plumes 
Microbial oxidation and precipitation of manganese at deep-sea hydrothermal vents are important oceanic biogeochemical processes, yet nothing is known about the types of microorganisms or mechanisms involved. Here we report isolation of a number of diverse spore-forming Mn(II)-oxidizing Bacillus species from Guaymas Basin, a deep-sea hydrothermal vent environment in the Gulf of California, where rapid microbially mediated Mn(II) oxidation was previously observed. mnxG multicopper oxidase genes involved in Mn(II) oxidation were amplified from all Mn(II)-oxidizing Bacillus spores isolated, suggesting that a copper-mediated mechanism of Mn(II) oxidation could be important at deep-sea hydrothermal vents. Phylogenetic analysis of 16S rRNA and mnxG genes revealed that while many of the deep-sea Mn(II)-oxidizing Bacillus species are very closely related to previously recognized isolates from coastal sediments, other organisms represent novel strains and clusters. The growth and Mn(II) oxidation properties of these Bacillus species suggest that in hydrothermal sediments they are likely present as spores that are active in oxidizing Mn(II) as it emerges from the seafloor.
PMCID: PMC1472353  PMID: 16672456

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