Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans

Prokaryotic microbes (bacteria and archaea) are the metabolic engine driving biogeochemical cylces that help to sustain conditions for life on Earth. Viruses target specific microbial metabolic pathways with auxiliary metabolic genes (AMGs) encoded in virus genomes.
Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans
Like

Share this post

Choose a social network to share with, or copy the URL to share elsewhere

This is a representation of how your post may appear on social media. The actual post will vary between social networks

Explore the Research

BioMed Central
BioMed Central BioMed Central

Prokaryotic-virus-encoded auxiliary metabolic genes throughout the global oceans - Microbiome

Background Prokaryotic microbes have impacted marine biogeochemical cycles for billions of years. Viruses also impact these cycles, through lysis, horizontal gene transfer, and encoding and expressing genes that contribute to metabolic reprogramming of prokaryotic cells. While this impact is difficult to quantify in nature, we hypothesized that it can be examined by surveying virus-encoded auxiliary metabolic genes (AMGs) and assessing their ecological context. Results We systematically developed a global ocean AMG catalog by integrating previously described and newly identified AMGs and then placed this catalog into ecological and metabolic contexts relevant to ocean biogeochemistry. From 7.6 terabases of Tara Oceans paired prokaryote- and virus-enriched metagenomic sequence data, we increased known ocean virus populations to 579,904 (up 16%). From these virus populations, we then conservatively identified 86,913 AMGs that grouped into 22,779 sequence-based gene clusters, 7248 (~ 32%) of which were not previously reported. Using our catalog and modeled data from mock communities, we estimate that ~ 19% of ocean virus populations carry at least one AMG. To understand AMGs in their metabolic context, we identified 340 metabolic pathways encoded by ocean microbes and showed that AMGs map to 128 of them. Furthermore, we identified metabolic “hot spots” targeted by virus AMGs, including nine pathways where most steps (≥ 0.75) were AMG-targeted (involved in carbohydrate, amino acid, fatty acid, and nucleotide metabolism), as well as other pathways where virus-encoded AMGs outnumbered cellular homologs (involved in lipid A phosphates, phosphatidylethanolamine, creatine biosynthesis, phosphoribosylamine-glycine ligase, and carbamoyl-phosphate synthase pathways). Conclusions Together, this systematically curated, global ocean AMG catalog and analyses provide a valuable resource and foundational observations to understand the role of viruses in modulating global ocean metabolisms and their biogeochemical implications. Video Abstract

 The search for a systematic catalog of auxiliary metabolic genes (AMGs) within marine viruses goes back over 20 years. The story of AMGs in viruses can be traced back to Sullivan's days as a graduate student and Debbie Lindell's time as a postdoc in the Chisholm lab at MIT, when he inadvertently identified photosynthesis genes in cyanophages (viruses that infect cyanobacteria) and thought they were contamination in the genomes. Debbie immediately saw them as a signature of co-evolution1. Debbie later showed that these genes were indeed transcribed and translated during infection2,3, which Jason Bragg then modeled physiological differences4

In the decades since sequencing technology and analytic advances have driven a surge in AMG studies across various ecosystems. Yet the lack of a systematically curated AMG catalog remained, thus hindering the integration of viruses into models to quantitatively assess their metabolic and biogeochemical impacts. Fortunately, five years prior to this study, global dsDNA catalog papers began to be published5,6,7, resulting in the identification of over 190,000 dsDNA viruses across the global oceans. For the first time, this presented a global ocean dataset that was deeply sequenced and curated for dsDNA viruses. It was against this backdrop that Funing Tian, then a PhD student in Microbiology who had received a University Fellowship from The Ohio State University, and James Wainaina, having just completed his graduate studies at the University of Western Australia (UWA), began working on this project. 

Funing Tian (Left), Zhiping Zhong (Center), and James Wainaina (Right) during a poster presentation of the global AMG catalog work at the Center of Microbiome Science (CoMS) MidWest Conference May 2022

The Ocean AMG project faced numerous challenges. First, despite the increase in AMG studies, the lack of standards for what constitutes a 'bona fide' AMG has prevented cross-study comparisons. This necessitated the development of standards for what could be 'conservatively' assigned as AMGs, a process that took almost a year and was further aided by new analytical tools by Kelly Wrighton lab8. After identifying ~22,000 AMG gene clusters, the second challenge was determining how to narrow down to the most biogeochemical important AMGs, without "cherry-picking" the dataset, this was the most challenging part of the project. We tried over half a dozen approaches to select a subset of biologically relevant AMGs that would be sufficient to highlight and discuss. We eventually focused on a few based on their metabolic functions, thanks in part to colleagues and co-authors (Cristina Howard-Verona and Garrett Smith) in the Sullivan lab as well, as co-author Steven Hallam, who had strong 'metabolic brains.' However, we confess we have just but scratched the surface of this catalog. Since the data is publicly available, it provides the scientific community with a catalog they can explore further. We look forward to the numerous subplots this dataset will reveal in the coming years, especially important in unraveling the role of viruses in ocean biogeochemical processes that has remained elusive to quantify.

There are several take-home messages from this paper. Firstly, given the avalanche of data from large consortia such as the Tara Ocean Expedition, it is crucial to have a systematic and scalable approach for analyzing the data and enabling cross-study comparisons. Secondly, reliable, updated, and maintained viral ecogenomics tools will be essential for continuously exploring and advancing omic data sets, especially within the marine ecosystem. Finally, this study would not have been possible without cross-disciplinary collaboration, teamwork, dogged determination despite scientific challenges, and an unwavering spirit; this was particularly important as it took over four years to get this work to publication.

What does the future hold for us, Funing Tian, now Dr. Tian is currently a Bioinformatician at the University of Chicago, where she focuses on bioinformatics analysis of single-cell multi-omics sequencing for asthma research. James has started his research group at the Woods Hole Oceanographic Institution Biology Department, where he  continues exploring the ecology and evolution of marine viruses with a particular focus on corals.

 Reference:

1.        Sullivan, M. B. et al. Prevalence and Evolution of Core Photosystem II Genes in Marine Cyanobacterial Viruses and Their Hosts. PLoS Biol. 4, e234 (2006).

2.        Lindell, D. et al. Transfer of photosynthesis genes to and from Prochlorococcus viruses. Proc. Natl. Acad. Sci. U. S. A. 101, 11013–11018 (2004).

3.        Lindell, D., Jaffe, J. D., Johnson, Z. I., Church, G. M. & Chisholm, S. W. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 438, 86–89 (2005).

4.        Bragg, J. G. & Chisholm, S. W. Modeling the fitness consequences of a cyanophage-encoded photosynthesis gene. PLoS One 3, 1–9 (2008).

5.        Brum, J. R. et al. Ocean Viral Communities. Science (80-. ). 348, 1261498-1–11 (2015).

6.        Roux, S. et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693 (2016).

7.        Gregory, A. C. et al. Marine DNA Viral Macro- and Microdiversity from Pole to Pole. Cell 177, 1109-1123.e14 (2019).

8.        Shaffer, M. et al. DRAM for distilling microbial metabolism to automate the curation of microbiome function. Nucleic Acids Res. 48, 8883–8900 (2020).

 

 

Please sign in or register for FREE

If you are a registered user on Research Communities by Springer Nature, please sign in

Follow the Topic

Biooceanography
Life Sciences > Biological Sciences > Ecology > Biooceanography
Environmental Sciences
Physical Sciences > Earth and Environmental Sciences > Environmental Sciences
Environmental Microbiology
Life Sciences > Biological Sciences > Microbiology > Environmental Microbiology
Virology
Life Sciences > Biological Sciences > Microbiology > Virology
  • Microbiome Microbiome

    This journal hopes to integrate researchers with common scientific objectives across a broad cross-section of sub-disciplines within microbial ecology. It covers studies of microbiomes colonizing humans, animals, plants or the environment, both built and natural or manipulated, as in agriculture.

Related Collections

With Collections, you can get published faster and increase your visibility.

Harnessing plant microbiomes to improve performance and mechanistic understanding

This is a Cross-Journal Collection with Microbiome, Environmental Microbiome, npj Science of Plants, and npj Biofilms and Microbiomes. Please click here to see the collection page for npj Science of Plants and npj Biofilms and Microbiomes.

Modern agriculture needs to sustainably increase crop productivity while preserving ecosystem health. As soil degradation, climate variability, and diminishing input efficiency continue to threaten agricultural outputs, there is a pressing need to enhance plant performance through ecologically-sound strategies. In this context, plant-associated microbiomes represent a powerful, yet underexploited, resource to improve plant vigor, nutrient acquisition, stress resilience, and overall productivity.

The plant microbiome—comprising bacteria, fungi, and other microorganisms inhabiting the rhizosphere, endosphere, and phyllosphere—plays a fundamental role in shaping plant physiology and development. Increasing evidence demonstrates that beneficial microbes mediate key processes such as nutrient solubilization and uptake, hormonal regulation, photosynthetic efficiency, and systemic resistance to (a)biotic stresses. However, to fully harness these capabilities, a mechanistic understanding of the molecular dialogues and functional traits underpinning plant-microbe interactions is essential.

Recent advances in multi-omics technologies, synthetic biology, and high-throughput functional screening have accelerated our ability to dissect these interactions at molecular, cellular, and system levels. Yet, significant challenges remain in translating these mechanistic insights into robust microbiome-based applications for agriculture. Core knowledge gaps include identifying microbial functions that are conserved across environments and hosts, understanding the signaling networks and metabolic exchanges between partners, and predicting microbiome assembly and stability under field conditions.

This Research Topic welcomes Original Research, Reviews, Perspectives, and Meta-analyses that delve into the functional and mechanistic basis of plant-microbiome interactions. We are particularly interested in contributions that integrate molecular microbiology, systems biology, plant physiology, and computational modeling to unravel the mechanisms by which microbial communities enhance plant performance and/or mechanisms employed by plant hosts to assemble beneficial microbiomes. Studies ranging from controlled experimental systems to applied field trials are encouraged, especially those aiming to bridge the gap between fundamental understanding and translational outcomes such as microbial consortia, engineered strains, or microbiome-informed management practices.

Ultimately, this collection aims to advance our ability to rationally design and apply microbiome-based strategies by deepening our mechanistic insight into how plants select beneficial microbiomes and in turn how microbes shape plant health and productivity.

This collection is open for submissions from all authors on the condition that the manuscript falls within both the scope of the collection and the journal it is submitted to.

All submissions in this collection undergo the relevant journal’s standard peer review process. Similarly, all manuscripts authored by a Guest Editor(s) will be handled by the Editor-in-Chief of the relevant journal. As an open access publication, participating journals levy an article processing fee (Microbiome, Environmental Microbiome). We recognize that many key stakeholders may not have access to such resources and are committed to supporting participation in this issue wherever resources are a barrier. For more information about what support may be available, please visit OA funding and support, or email OAfundingpolicy@springernature.com or the Editor-in-Chief of the journal where the article is being submitted.

Collection policies for Microbiome and Environmental Microbiome:

Please refer to this page. Please only submit to one journal, but note authors have the option to transfer to another participating journal following the editors’ recommendation.

Collection policies for npj Science of Plants and npj Biofilms and Microbiomes:

Please refer to npj's Collection policies page for full details.

Publishing Model: Open Access

Deadline: Jun 01, 2026

Microbiome and Reproductive Health

Microbiome is calling for submissions to our Collection on Microbiome and Reproductive Health.

Our understanding of the intricate relationship between the microbiome and reproductive health holds profound translational implications for fertility, pregnancy, and reproductive disorders. To truly advance this field, it is essential to move beyond descriptive and associative studies and focus on mechanistic research that uncovers the functional underpinnings of the host–microbiome interface. Such studies can reveal how microbial communities influence reproductive physiology, including hormonal regulation, immune responses, and overall reproductive health.

Recent advances have highlighted the role of specific bacterial populations in both male and female fertility, as well as their impact on pregnancy outcomes. For example, the vaginal microbiome has been linked to preterm birth, while emerging evidence suggests that gut microbiota may modulate reproductive hormone levels. These insights underscore the need for research that explores how and why these microbial influences occur.

Looking ahead, the potential for breakthroughs is immense. Mechanistic studies have the power to drive the development of microbiome-based therapies that address infertility, improve pregnancy outcomes, and reduce the risk of reproductive diseases. Incorporating microbiome analysis into reproductive health assessments could transform clinical practice and, by deepening our understanding of host–microbiome mechanisms, lay the groundwork for personalized medicine in gynecology and obstetrics.

We invite researchers to contribute to this Special Collection on Microbiome and Reproductive Health. Submissions should emphasize functional and mechanistic insights into the host–microbiome relationship. Topics of interest include, but are not limited to:

- Microbiome and infertility

- Vaginal microbiome and pregnancy outcomes

- Gut microbiota and reproductive hormones

- Microbial influences on menstrual health

- Live biotherapeutics and reproductive health interventions

- Microbiome alterations as drivers of reproductive disorders

- Environmental factors shaping the microbiome

- Intergenerational microbiome transmission

This Collection supports and amplifies research related to SDG 3, Good Health and Well-Being.

All submissions in this collection undergo the journal’s standard peer review process. As an open access publication, this journal levies an article processing fee (details here). We recognize that many key stakeholders may not have access to such resources and are committed to supporting participation in this issue wherever resources are a barrier. For more information about what support may be available, please visit OA funding and support, or email OAfundingpolicy@springernature.com or the Editor-in-Chief.

Publishing Model: Open Access

Deadline: Jun 16, 2026