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Abstract BackgroundViruses, the majority of which are uncultivated, are among the most abundant biological entities on Earth. From altering microbial physiology to driving community dynamics, viruses are fundamental members of microbiomes. While the number of studies leveraging viral metagenomics (viromics) for studying uncultivated viruses is growing, standards for viromics research are lacking. Viromics can utilize computational discovery of viruses from total metagenomes of all community members (hereafter metagenomes) or use physical separation of virus-specific fractions (hereafter viromes). However, differences in the recovery and interpretation of viruses from metagenomes and viromes obtained from the same samples remain understudied. ResultsHere, we compare viral communities from paired viromes and metagenomes obtained from 60 diverse samples across human gut, soil, freshwater, and marine ecosystems. Overall, viral communities obtained from viromes had greater species richness and total viral genome abundances than those obtained from metagenomes, although there were some exceptions. Despite this, metagenomes still contained many viral genomes not detected in viromes. We also found notable differences in the predicted lytic state of viruses detected in viromes vs metagenomes at the time of sequencing. Other forms of variation observed include genome presence/absence, genome quality, and encoded protein content between viromes and metagenomes, but the magnitude of these differences varied by environment. ConclusionsOverall, our results show that the choice of method can lead to differing interpretations of viral community ecology. We suggest that the choice of whether to target a metagenome or virome to study viral communities should be dependent on the environmental context and ecological questions being asked. However, our overall recommendation to researchers investigating viral ecology and evolution is to pair both approaches to maximize their respective benefits. 

Abstract Viruses are ubiquitous in deep-sea hydrothermal vents, where they influence microbial communities and biogeochemistry. Yet, viral ecology and evolution remain understudied in these environments. Here, we identify 49,962 viruses from 52 globally distributed hydrothermal vent samples (10 plume, 40 deposit, and 2 diffuse flow metagenomes), and reconstruct 5708 viral metagenome-assembled genomes, the majority of which were bacteriophages. Hydrothermal viruses were largely endemic, however, some viruses were shared between geographically separated vents, predominantly between the Lau Basin and Brothers Volcano in the Pacific Ocean. Geographically distant viruses shared proteins related to core functions such as structural proteins, and rarely, proteins of auxiliary functions involved in processes such as fermentation and cobalamin biosynthesis. Common microbial hosts of viruses included members of Campylobacterota, Alpha-, and Gammaproteobacteria in deposits, and Gammaproteobacteria in plumes. Campylobacterota- and Gammaproteobacteria-infecting viruses reflected variations in hydrothermal chemistry and functional redundancy in their predicted microbial hosts, suggesting that hydrothermal geology is a driver of viral ecology and coevolution of viruses and hosts. Our results indicate that viral ecology and evolution in globally distributed hydrothermal vents is shaped by endemism and thus may have increased susceptibility to the negative impacts of deep-sea mining and anthropogenic change in ocean ecosystems. 

Abstract Microorganisms play vital roles in sulfur cycling through the oxidation of elemental sulfur and reduction of sulfite. These metabolisms are catalyzed by dissimilatory sulfite reductases (Dsr) functioning in either the reductive or reverse, oxidative direction. Dsr-mediated sulfite reduction is an ancient metabolism proposed to have fueled energy metabolism in some of Earth’s earliest microorganisms, whereas sulfur oxidation is believed to have evolved later in association with the widespread availability of oxygen on Earth. Organisms are generally believed to carry out either the reductive or oxidative pathway, yet organisms from diverse phyla have been discovered with gene combinations that implicate them in both pathways. A comprehensive investigation into the metabolisms of these phyla regarding Dsr is currently lacking. Here, we selected one of these phyla, the metabolically versatile candidate phylum SAR324, to study the ecology and evolution of Dsr-mediated metabolism. We confirmed that diverse SAR324 encode genes associated with reductive Dsr, oxidative Dsr, or both. Comparative analyses with other Dsr-encoding bacterial and archaeal phyla revealed that organisms encoding both reductive and oxidative Dsr proteins are constrained to a few phyla. Further, DsrAB sequences from genomes belonging to these phyla are phylogenetically positioned at the interface between well-defined oxidative and reductive bacterial clades. The phylogenetic context and dsr gene content in these organisms points to an evolutionary transition event that ultimately gave way to oxidative Dsr-mediated metabolism. Together, this research suggests that SAR324 and other phyla with mixed dsr gene content are associated with the evolution and origins of Dsr-mediated sulfur oxidation. 

Abstract BackgroundWhen deep-sea hydrothermal fluids mix with cold oxygenated fluids, minerals precipitate out of solution and form hydrothermal deposits. These actively venting deep-sea hydrothermal deposits support a rich diversity of thermophilic microorganisms which are involved in a range of carbon, sulfur, nitrogen, and hydrogen metabolisms. Global patterns of thermophilic microbial diversity in deep-sea hydrothermal ecosystems have illustrated the strong connectivity between geological processes and microbial colonization, but little is known about the genomic diversity and physiological potential of these novel taxa. Here we explore this genomic diversity in 42 metagenomes from four deep-sea hydrothermal vent fields and a deep-sea volcano collected from 2004 to 2018 and document their potential implications in biogeochemical cycles. ResultsOur dataset represents 3635 metagenome-assembled genomes encompassing 511 novel and recently identified genera from deep-sea hydrothermal settings. Some of the novel bacterial (107) and archaeal genera (30) that were recently reported from the deep-sea Brothers volcano were also detected at the deep-sea hydrothermal vent fields, while 99 bacterial and 54 archaeal genera were endemic to the deep-sea Brothers volcano deposits. We report some of the first examples of medium- (≥ 50% complete, ≤ 10% contaminated) to high-quality (> 90% complete, < 5% contaminated) MAGs from phyla and families never previously identified, or poorly sampled, from deep-sea hydrothermal environments. We greatly expand the novel diversity of Thermoproteia, Patescibacteria (Candidate Phyla Radiation, CPR), and Chloroflexota found at deep-sea hydrothermal vents and identify a small sampling of two potentially novel phyla, designated JALSQH01 and JALWCF01. Metabolic pathway analysis of metagenomes provides insights into the prevalent carbon, nitrogen, sulfur, and hydrogen metabolic processes across all sites and illustrates sulfur and nitrogen metabolic “handoffs” in community interactions. We confirm that Campylobacteria and Gammaproteobacteria occupy similar ecological guilds but their prevalence in a particular site is driven by shifts in the geochemical environment. ConclusionOur study of globally distributed hydrothermal vent deposits provides a significant expansion of microbial genomic diversity associated with hydrothermal vent deposits and highlights the metabolic adaptation of taxonomic guilds. Collectively, our results illustrate the importance of comparative biodiversity studies in establishing patterns of shared phylogenetic diversity and physiological ecology, while providing many targets for enrichment and cultivation of novel and endemic taxa. 

Abstract BackgroundAdvances in microbiome science are being driven in large part due to our ability to study and infer microbial ecology from genomes reconstructed from mixed microbial communities using metagenomics and single-cell genomics. Such omics-based techniques allow us to read genomic blueprints of microorganisms, decipher their functional capacities and activities, and reconstruct their roles in biogeochemical processes. Currently available tools for analyses of genomic data can annotate and depict metabolic functions to some extent; however, no standardized approaches are currently available for the comprehensive characterization of metabolic predictions, metabolite exchanges, microbial interactions, and microbial contributions to biogeochemical cycling. ResultsWe present METABOLIC (METabolic And BiogeOchemistry anaLyses In miCrobes), a scalable software to advance microbial ecology and biogeochemistry studies using genomes at the resolution of individual organisms and/or microbial communities. The genome-scale workflow includes annotation of microbial genomes, motif validation of biochemically validated conserved protein residues, metabolic pathway analyses, and calculation of contributions to individual biogeochemical transformations and cycles. The community-scale workflow supplements genome-scale analyses with determination of genome abundance in the microbiome, potential microbial metabolic handoffs and metabolite exchange, reconstruction of functional networks, and determination of microbial contributions to biogeochemical cycles. METABOLIC can take input genomes from isolates, metagenome-assembled genomes, or single-cell genomes. Results are presented in the form of tables for metabolism and a variety of visualizations including biogeochemical cycling potential, representation of sequential metabolic transformations, community-scale microbial functional networks using a newly defined metric “MW-score” (metabolic weight score), and metabolic Sankey diagrams. METABOLIC takes ~ 3 h with 40 CPU threads to process ~ 100 genomes and corresponding metagenomic reads within which the most compute-demanding part of hmmsearch takes ~ 45 min, while it takes ~ 5 h to complete hmmsearch for ~ 3600 genomes. Tests of accuracy, robustness, and consistency suggest METABOLIC provides better performance compared to other software and online servers. To highlight the utility and versatility of METABOLIC, we demonstrate its capabilities on diverse metagenomic datasets from the marine subsurface, terrestrial subsurface, meadow soil, deep sea, freshwater lakes, wastewater, and the human gut. ConclusionMETABOLIC enables the consistent and reproducible study of microbial community ecology and biogeochemistry using a foundation of genome-informed microbial metabolism, and will advance the integration of uncultivated organisms into metabolic and biogeochemical models. METABOLIC is written in Perl and R and is freely available under GPLv3 athttps://github.com/AnantharamanLab/METABOLIC. 

ABSTRACT Viruses are ubiquitous on Earth and are keystone components of environments, ecosystems, and human health. Yet, viruses remain poorly studied because most cannot be isolated in a laboratory. In the field of biogeochemistry, which aims to understand the interactions between biology, geology, and chemistry, there is progress to be made in understanding the different roles played by viruses in nutrient cycling, food webs, and elemental transformations. In this commentary, we outline current microbial ecology frameworks for understanding biogeochemical cycling in aquatic ecosystems. Next, we review some existing experimental and computational techniques that are enabling us to study the role of viruses in biogeochemical cycling, using examples from aquatic environments. Finally, we provide a conceptual model that balances limitations of computational tools when combined with biogeochemistry and ecological data. We envision meeting the grand challenge of understanding how viruses impact biogeochemical cycling by using a multifaceted approach to viral ecology.