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1.  Comparative metagenomic analyses reveal viral-induced shifts of host metabolism towards nucleotide biosynthesis 
Microbiome  2014;2:9.
Background
Viral genomes often contain metabolic genes that were acquired from host genomes (auxiliary genes). It is assumed that these genes are fixed in viral genomes as a result of a selective force, favoring viruses that acquire specific metabolic functions. While many individual auxiliary genes were observed in viral genomes and metagenomes, there is great importance in investigating the abundance of auxiliary genes and metabolic functions in the marine environment towards a better understanding of their role in promoting viral reproduction.
Results
In this study, we searched for enriched viral auxiliary genes and mapped them to metabolic pathways. To initially identify enriched auxiliary genes, we analyzed metagenomic microbial reads from the Global Ocean Survey (GOS) dataset that were characterized as viral, as well as marine virome and microbiome datasets from the Line Islands. Viral-enriched genes were mapped to a “global metabolism network” that comprises all KEGG metabolic pathways. Our analysis of the viral-enriched pathways revealed that purine and pyrimidine metabolism pathways are among the most enriched pathways. Moreover, many other viral-enriched metabolic pathways were found to be closely associated with the purine and pyrimidine metabolism pathways. Furthermore, we observed that sequential reactions are promoted in pathways having a high proportion of enriched genes. In addition, these enriched genes were found to be of modular nature, participating in several pathways.
Conclusions
Our naïve metagenomic analyses strongly support the well-established notion that viral auxiliary genes promote viral replication via both degradation of host DNA and RNA as well as a shift of the host metabolism towards nucleotide biosynthesis, clearly indicating that comparative metagenomics can be used to understand different environments and systems without prior knowledge of pathways involved.
doi:10.1186/2049-2618-2-9
PMCID: PMC4022391  PMID: 24666644
Metabolic networks; Metabolism; Nucleotide biosynthesis; Phage; Virus
2.  Global abundance of microbial rhodopsins 
The ISME Journal  2012;7(2):448-451.
Photochemical reaction centers and rhodopsins are the only phototrophic mechanisms known to have evolved on Earth. The minimal cost of bearing a rhodopsin-based phototrophic mechanism in comparison to maintaining a photochemical reaction center suggests that rhodopsin is the more abundant of the two. We tested this hypothesis by conducting a global abundance calculation of phototrophic mechanisms from 116 marine and terrestrial microbial metagenomes. On average, 48% of the cells from which these metagenomes were generated harbored a rhodopsin gene, exceeding the reaction center abundance by threefold. Evidence from metatranscriptomic data suggests that this genomic potential is realized to a substantial extent, at least for the small-sized (>0.8 μm) of microbial fractions.
doi:10.1038/ismej.2012.112
PMCID: PMC3554412  PMID: 23051692
metagenomics; phototrophy; rhodopsin
3.  Viral clones from the GOS expedition with an unusual photosystem-I gene cassette organization 
The ISME Journal  2012;6(8):1617-1620.
Cyanobacteria have a key role in marine photosynthesis, which contributes to the global carbon cycle and to the world oxygen supply. Genes encoding for photosystem-II (PSII) and photosystem-I (PSI) reaction centers are found in different cyanophage genomes, and it was suggested that the horizontal transfer of these genes might be involved in increasing phage fitness. We have further analyzed a rare viral Global Ocean Sampling (GOS) clone containing PSI genes. This clone contains the unusual PSI gene organization psaD->C->A, as opposed to the more frequently observed viral psaJF->C->A->B->K->E->D organization, and was detected only once in the GOS metagenome. Our analyses identified more occurrences with similar arrangement and indicate that this PSI viral gene organization (now psaD->C->A->B), although rare, is authentic and represents a new PSI gene arrangement.
doi:10.1038/ismej.2012.23
PMCID: PMC3400403  PMID: 22456446
photosystem I; phage; cyanobacteria; Synechococcus; Prochlorococcus
4.  Potential for phosphite and phosphonate utilization by Prochlorococcus 
The ISME Journal  2011;6(4):827-834.
Phosphonates (Pn) are diverse organic phosphorus (P) compounds containing C–P bonds and comprise up to 25% of the high-molecular weight dissolved organic P pool in the open ocean. Pn bioavailability was suggested to influence markedly bacterial primary production in low-P areas. Using metagenomic data from the Global Ocean Sampling expedition, we show that the main potential microbial contributor in Pn utilization in oceanic surface water is the globally important marine primary producer Prochlorococcus. Moreover, a number of Prochlorococcus strains contain two distinct putative Pn uptake operons coding for ABC-type Pn transporters. On the basis of microcalorimetric measurements, we find that each of the two different putative Pn-binding protein (PhnD) homologs transcribed from these operons possesses different Pn- as well as inorganic phosphite-binding specificities. Our results suggest that Prochlorococcus adapt to low-P environments by increasing the number of Pn transporters with different specificities towards phosphite and different Pns.
doi:10.1038/ismej.2011.149
PMCID: PMC3309357  PMID: 22011717
phosphonate; phosphite; Prochlorococcus; phosphate
5.  Microbial rhodopsins on leaf surfaces of terrestrial plants 
Environmental microbiology  2011;14(1):140-146.
Summary
The above-ground surfaces of terrestrial plants, the phyllosphere, comprise the main interface between the terrestrial biosphere and solar radiation. It is estimated to host up to 1026 microbial cells that may intercept part of the photon flux impinging on the leaves. Based on 454-pyrosequencing-generated metagenome data, we report on the existence of diverse microbial rhodopsins in five distinct phyllospheres from tamarisk (Tamarix nilotica), soybean (Glycine max), Arabidopsis (Arabidopsis thaliana), clover (Trifolium repens) and rice (Oryza sativa). Our findings, for the first time describing microbial rhodopsins from non-aquatic habitats, point towards the potential coexistence of microbial rhodopsin-based phototrophy and plant chlorophyll-based photosynthesis, with the different pigments absorbing non-overlapping fractions of the light spectrum.
doi:10.1111/j.1462-2920.2011.02554.x
PMCID: PMC3608849  PMID: 21883799
6.  Cyanophage tRNAs may have a role in cross-infectivity of oceanic Prochlorococcus and Synechococcus hosts 
The ISME Journal  2011;6(3):619-628.
Marine cyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic prokaryotes in oceanic environments, and are key contributors to global CO2 fixation, chlorophyll biomass and primary production. Cyanophages, viruses infecting cyanobacteria, are a major force in the ecology of their hosts. These phages contribute greatly to cyanobacterial mortality, therefore acting as a powerful selective force upon their hosts. Phage reproduction is based on utilization of the host transcription and translation mechanisms; therefore, differences in the G+C genomic content between cyanophages and their hosts could be a limiting factor for the translation of cyanophage genes. On the basis of comprehensive genomic analyses conducted in this study, we suggest that cyanophages of the Myoviridae family, which can infect both Prochlorococcus and Synechococcus, overcome this limitation by carrying additional sets of tRNAs in their genomes accommodating AT-rich codons. Whereas the tRNA genes are less needed when infecting their Prochlorococcus hosts, which possess a similar G+C content to the cyanophage, the additional tRNAs may increase the overall translational efficiency of their genes when infecting a Synechococcus host (with high G+C content), therefore potentially enabling the infection of multiple hosts.
doi:10.1038/ismej.2011.146
PMCID: PMC3280135  PMID: 22011720
codon usage; cross-infectivity; marine cyanophages; Prochlorococcus; Synechococcus; tRNA
7.  Marine cyanophages: tinkering with the electron transport chain 
The ISME Journal  2011;5(10):1568-1570.
doi:10.1038/ismej.2011.43
PMCID: PMC3176516  PMID: 21509045
8.  Comparative metagenomics of microbial traits within oceanic viral communities 
The ISME Journal  2011;5(7):1178-1190.
Viral genomes often contain genes recently acquired from microbes. In some cases (for example, psbA) the proteins encoded by these genes have been shown to be important for viral replication. In this study, using a unique search strategy on the Global Ocean Survey (GOS) metagenomes in combination with marine virome and microbiome pyrosequencing-based datasets, we characterize previously undetected microbial metabolic capabilities concealed within the genomes of uncultured marine viral communities. A total of 34 microbial gene families were detected on 452 viral GOS scaffolds. The majority of auxiliary metabolic genes found on these scaffolds have never been reported in phages. Host genes detected in viruses were mainly divided between genes encoding for different energy metabolism pathways, such as electron transport and newly identified photosystem genes, or translation and post-translation mechanism related. Our findings suggest previously undetected ways, in which marine phages adapt to their hosts and improve their fitness, including translation and post-translation level control over the host rather than the already known transcription level control.
doi:10.1038/ismej.2011.2
PMCID: PMC3146289  PMID: 21307954
cyanophage; gene transfer; metagenomics; photosynthesis; viral–host interactions
9.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/9505d865-7e1e-4f1e-84a0-f568d8552414.
doi:10.1371/annotation/9505d865-7e1e-4f1e-84a0-f568d8552414
PMCID: PMC3346701
10.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/590a9ab4-5736-4f11-a93a-a31f25990d96.
doi:10.1371/annotation/590a9ab4-5736-4f11-a93a-a31f25990d96
PMCID: PMC3346702
11.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/a260c562-9d55-452e-84fa-f33ce59b9704.
doi:10.1371/annotation/a260c562-9d55-452e-84fa-f33ce59b9704
PMCID: PMC3346703
12.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/a9234cc3-a14f-4c3f-8be6-645bfeca2b6c.
doi:10.1371/annotation/a9234cc3-a14f-4c3f-8be6-645bfeca2b6c
PMCID: PMC3346704
13.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/6830e1ff-b565-4054-bae6-02939f625cfe.
doi:10.1371/annotation/6830e1ff-b565-4054-bae6-02939f625cfe
PMCID: PMC3346705
14.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/fe6ae2ff-6778-4581-8d52-4aba3534c99f.
doi:10.1371/annotation/fe6ae2ff-6778-4581-8d52-4aba3534c99f
PMCID: PMC3346706
15.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/571dcbb4-cac9-4c84-9f9e-27cc87ceed0e.
doi:10.1371/annotation/571dcbb4-cac9-4c84-9f9e-27cc87ceed0e
PMCID: PMC3346707
16.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/05d3c1ef-0aad-4592-ab8d-6863fbdf73f9.
doi:10.1371/annotation/05d3c1ef-0aad-4592-ab8d-6863fbdf73f9
PMCID: PMC3346708
17.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/48a18f09-0a1a-469e-8c0d-b352e80200bc.
doi:10.1371/annotation/48a18f09-0a1a-469e-8c0d-b352e80200bc
PMCID: PMC3346709
18.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/65474650-89c5-4b56-80e8-6e513347d3d7.
doi:10.1371/annotation/65474650-89c5-4b56-80e8-6e513347d3d7
PMCID: PMC3346710
19.  Correction: The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2012;10(5):10.1371/annotation/52943e21-9d9d-4a2a-ba23-942bd6f01716.
doi:10.1371/annotation/52943e21-9d9d-4a2a-ba23-942bd6f01716
PMCID: PMC4188450
20.  The Light-Driven Proton Pump Proteorhodopsin Enhances Bacterial Survival during Tough Times 
PLoS Biology  2010;8(4):e1000359.
Recently, it has been discovered that many microorganisms previously thought to be light-independent actually make use of sunlight for growth and survival. Newly reported work suggests some of the specific mechanisms involved.
doi:10.1371/journal.pbio.1000359
PMCID: PMC2860490  PMID: 20436957
21.  Comparative classification of species and the study of pathway evolution based on the alignment of metabolic pathways 
BMC Bioinformatics  2010;11(Suppl 1):S38.
Background
Pathways provide topical descriptions of cellular circuitry. Comparing analogous pathways reveals intricate insights into individual functional differences among species. While previous works in the field performed genomic comparisons and evolutionary studies that were based on specific genes or proteins, whole genomic sequence, or even single pathways, none of them described a genomic system level comparative analysis of metabolic pathways. In order to properly implement such an analysis one should overcome two specific challenges: how to combine the effect of many pathways under a unified framework and how to appropriately analyze co-evolution of pathways.
Here we present a computational approach for solving these two challenges. First, we describe a comprehensive, scalable, information theory based computational pipeline that calculates pathway alignment information and then compiles it in a novel manner that allows further analysis. This approach can be used for building phylogenies and for pointing out specific differences that can then be analyzed in depth. Second, we describe a new approach for comparing the evolution of metabolic pathways. This approach can be used for detecting co-evolutionary relationships between metabolic pathways.
Results
We demonstrate the advantages of our approach by applying our pipeline to data from the MetaCyc repository (which includes a total of 205 organisms and 660 metabolic pathways). Our analysis revealed several surprising biological observations. For example, we show that the different habitats in which Archaea organisms reside are reflected by a pathway based phylogeny. In addition, we discover two striking clusters of metabolic pathways, each cluster includes pathways that have very similar evolution.
Conclusion
We demonstrate that distance measures that are based on the topology and the content of metabolic networks are useful for studying evolution and co-evolution.
doi:10.1186/1471-2105-11-S1-S38
PMCID: PMC3009510  PMID: 20122211
22.  BchY-Based Degenerate Primers Target All Types of Anoxygenic Photosynthetic Bacteria in a Single PCR▿ † ‡  
Applied and Environmental Microbiology  2009;75(23):7556-7559.
To detect anoxygenic bacteria containing either type 1 or type 2 photosynthetic reaction centers in a single PCR, we designed a degenerate primer set based on the bchY gene. The new primers were validated in silico using the GenBank nucleotide database as well as by PCR on pure strains and environmental DNA.
doi:10.1128/AEM.01014-09
PMCID: PMC2786397  PMID: 19801482
23.  Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes 
Environmental Microbiology  2009;11(2):289-299.
Sulfur-oxidizing prokaryotes (SOP) catalyse a central step in the global S-cycle and are of major functional importance for a variety of natural and engineered systems, but our knowledge on their actual diversity and environmental distribution patterns is still rather limited. In this study we developed a specific PCR assay for the detection of dsrAB that encode the reversely operating sirohaem dissimilatory sulfite reductase (rDSR) and are present in many but not all published genomes of SOP. The PCR assay was used to screen 42 strains of SOP (most without published genome sequence) representing the recognized diversity of this guild. For 13 of these strains dsrAB was detected and the respective PCR product was sequenced. Interestingly, most dsrAB-encoding SOP are capable of forming sulfur storage compounds. Phylogenetic analysis demonstrated largely congruent rDSR and 16S rRNA consensus tree topologies, indicating that lateral transfer events did not play an important role in the evolutionary history of known rDSR. Thus, this enzyme represents a suitable phylogenetic marker for diversity analyses of sulfur storage compound-exploiting SOP in the environment. The potential of this new functional gene approach was demonstrated by comparative sequence analyses of all dsrAB present in published metagenomes and by applying it for a SOP census in selected marine worms and an alkaline lake sediment.
doi:10.1111/j.1462-2920.2008.01760.x
PMCID: PMC2702494  PMID: 18826437
24.  A supervised learning approach for taxonomic classification of core-photosystem-II genes and transcripts in the marine environment 
BMC Genomics  2009;10:229.
Background
Cyanobacteria of the genera Synechococcus and Prochlorococcus play a key role in marine photosynthesis, which contributes to the global carbon cycle and to the world oxygen supply. Recently, genes encoding the photosystem II reaction center (psbA and psbD) were found in cyanophage genomes. This phenomenon suggested that the horizontal transfer of these genes may be involved in increasing phage fitness. To date, a very small percentage of marine bacteria and phages has been cultured. Thus, mapping genomic data extracted directly from the environment to its taxonomic origin is necessary for a better understanding of phage-host relationships and dynamics.
Results
To achieve an accurate and rapid taxonomic classification, we employed a computational approach combining a multi-class Support Vector Machine (SVM) with a codon usage position specific scoring matrix (cuPSSM). Our method has been applied successfully to classify core-photosystem-II gene fragments, including partial sequences coming directly from the ocean, to seven different taxonomic classes. Applying the method on a large set of DNA and RNA psbA clones from the Mediterranean Sea, we studied the distribution of cyanobacterial psbA genes and transcripts in their natural environment. Using our approach, we were able to simultaneously examine taxonomic and ecological distributions in the marine environment.
Conclusion
The ability to accurately classify the origin of individual genes and transcripts coming directly from the environment is of great importance in studying marine ecology. The classification method presented in this paper could be applied further to classify other genes amplified from the environment, for which training data is available.
doi:10.1186/1471-2164-10-229
PMCID: PMC2696472  PMID: 19445709
25.  Novel Primers Reveal Wider Diversity among Marine Aerobic Anoxygenic Phototrophs†  
Applied and Environmental Microbiology  2005;71(12):8958-8962.
Aerobic anoxygenic phototrophic bacteria (AAnPs) were previously proposed to account for up to 11% of marine bacterioplankton and to potentially have great ecological importance in the world's oceans. Our data show that previously used primers based on the M subunit of anoxygenic photosynthetic reaction center genes (pufM) do not comprehensively identify the diversity of AAnPs in the ocean. We have designed and tested a new set of pufM-specific primers and revealed several new AAnP variants in environmental DNA samples and genomic libraries.
doi:10.1128/AEM.71.12.8958-8962.2005
PMCID: PMC1317425  PMID: 16332899

Results 1-25 (28)