Microbes in marine sediments represent a large portion of the biosphere, and resolving their ecology is crucial for understanding global ocean processes. Single-gene diversity surveys have revealed several uncultured lineages that are widespread in ocean sediments and whose ecological roles are unknown, and advancements in the computational analysis of increasingly large genomic data sets have made it possible to reconstruct individual genomes from complex microbial communities. Using these metagenomic approaches to characterize sediments is transforming our view of microbial communities on the ocean floor and the biodiversity of the planet. In recent years, marine sediments have been a prominent source of new lineages in the tree of life. The incorporation of these lineages into existing phylogenies has revealed that many belong to distinct phyla, including archaeal phyla that are advancing our understanding of the origins of cellular complexity and eukaryotes. Detailed comparisons of the metabolic potentials of these new lineages have made it clear that uncultured bacteria and archaea are capable of mediating key previously undescribed steps in carbon and nutrient cycling. Expected final online publication date for the Annual Review of Marine Science, Volume 13 is January 3, 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
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Expansive microbial metabolic versatility and biodiversity in dynamic Guaymas Basin hydrothermal sediments
Microbes in Guaymas Basin (Gulf of California) hydrothermal sediments thrive on hydrocarbons and sulfur and experience steep, fluctuating temperature and chemical gradients. The functional capacities of communities inhabiting this dynamic habitat are largely unknown. Here, we reconstructed 551 genomes from hydrothermally influenced, and nearby cold sediments belonging to 56 phyla (40 uncultured). These genomes comprise 22 unique lineages, including five new candidate phyla. In contrast to findings from cold hydrocarbon seeps, hydrothermal-associated communities are more diverse and archaea dominate over bacteria. Genome-based metabolic inferences provide first insights into the ecological niches of these uncultured microbes, including methane cycling in new Crenarchaeota and alkane utilization in ANME-1. These communities are shaped by a high biodiversity, partitioning among nitrogen and sulfur pathways and redundancy in core carbon-processing pathways. The dynamic sediments select for distinctive microbial communities that stand out by expansive biodiversity, and open up new physiological perspectives into hydrothermal ecosystem function.
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- Award ID(s):
- 1753661
- NSF-PAR ID:
- 10081391
- Date Published:
- Journal Name:
- Nature communications
- Volume:
- 9
- Issue:
- 4999
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Background When 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.
Results Our 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.
Conclusion Our 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.
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Abstract Deltaproteobacteria, now proposed to be the phyla Desulfobacterota, Myxococcota, and SAR324, are ubiquitous in marine environments and play essential roles in global carbon, sulfur, and nutrient cycling. Despite their importance, our understanding of these bacteria is biased towards cultured organisms. Here we address this gap by compiling a genomic catalog of 1 792 genomes, including 402 newly reconstructed and characterized metagenome-assembled genomes (MAGs) from coastal and deep-sea sediments. Phylogenomic analyses reveal that many of these novel MAGs are uncultured representatives of Myxococcota and Desulfobacterota that are understudied. To better characterize Deltaproteobacteria diversity, metabolism, and ecology, we clustered ~1 500 genomes based on the presence/absence patterns of their protein families. Protein content analysis coupled with large-scale metabolic reconstructions separates eight genomic clusters of Deltaproteobacteria with unique metabolic profiles. While these eight clusters largely correspond to phylogeny, there are exceptions where more distantly related organisms appear to have similar ecological roles and closely related organisms have distinct protein content. Our analyses have identified previously unrecognized roles in the cycling of methylamines and denitrification among uncultured Deltaproteobacteria. This new view of Deltaproteobacteria diversity expands our understanding of these dominant bacteria and highlights metabolic abilities across diverse taxa.
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The surficial hydrothermal sediments of Guaymas Basin harbor complex microbial communities where oxidative and reductive nitrogen, sulfur, and carbon-cycling populations and processes overlap and coexist. Here, we resolve microbial community profiles in hydrothermal sediment cores of Guaymas Basin on a scale of 2 millimeters, using Denaturing Gradient Gel Electrophoresis (DGGE) to visualize the rapid downcore changes among dominant bacteria and archaea. DGGE analysis of bacterial 16S rRNA gene amplicons identified free-living and syntrophic deltaproteobacterial sulfate-reducing bacteria, fermentative Cytophagales, members of the Chloroflexi (Thermoflexia), Aminicenantes, and uncultured sediment clades. The DGGE pattern indicates a gradually changing downcore community structure where small changes on a 2-millimeter scale accumulate to significantly changing populations within the top 4 cm sediment layer. Functional gene DGGE analyses identified anaerobic methane-oxidizing archaea (ANME) based on methyl-coenzyme M reductase genes, and members of the Betaproteobacteria and Thaumarchaeota based on bacterial and archaeal ammonia monooxygenase genes, respectively. The co-existence and overlapping habitat range of aerobic, nitrifying, sulfate-reducing and fermentative bacteria and archaea, including thermophiles, in the surficial sediments is consistent with dynamic redox and thermal gradients that sustain highly complex microbial communities in the hydrothermal sediments of Guaymas Basin.more » « less
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null (Ed.)Abstract Background Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Results Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria , the middle and lower parts by anoxygenic purple sulfur bacteria ( Chromatiales ) and green sulfur bacteria ( Chlorobiales ), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation and photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi . Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp . Conclusions The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi -affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi . The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/s41467-018-07418-0
