The bacterial sulfur cycle in expanding dysoxic and euxinic marine waters

Dysoxic marine waters (DMW, <1 M oxygen) are currently expanding in volume in the oceans, which has biogeochemical, ecological, and societal consequences on a global scale. In these environments, distinct bacteria drive an active sulfur cycle, which has only recently been recognized for openocean DMW. This review summarizes the current knowledge on these sulfurcycling bacteria. Critical bottlenecks and questions for future research are specifically addressed. Sulfatereducing bacteria (SRB) are core members of DMW. However, their roles are not entirely clear, and they remain largely uncultured. We found support for their remarkable diversity and taxonomic novelty by mining metagenomeassembled genomes from the Black Sea as model ecosystem. We highlight recent insights into the metabolism of key sulfuroxidizing SUP05 and Sulfurimonas bacteria, and discuss the probable involvement of uncultivated SAR324 and BSGSO2 bacteria in sulfur oxidation. Uncultivated Marinimicrobia bacteria with a presumed organoheterotrophic metabolism are abundant in DMW. Like SRB, they may use specific molybdoenzymes to conserve energy from the oxidation, reduction or disproportionation of sulfur cycle intermediates such as S0 and thiosulfate, produced from the oxidation of sulfide. However, this complex network of reactions is yet to be constrained quantitatively. This article is protected by copyright. All rights reserved.SIAM Gravitation grant 024.002.002 to AJMS and JSSD of the Netherlands Ministry of Education, Culture and Science and the Netherlands Organisation for Scientific Research (NWO). BED and FABvM were supported by the NWO Vidi grant 864.14.004. BED was supported by the European Research Council (ERC) Consolidator grant 865694: DiversiPHIinfo:eu-repo/semantics/publishedVersio

Sulfur oxidation genes in diverse deep-sea viruses

Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of AAAS for personal use, not for redistribution. The definitive version was published in Science 344 (2014): 757-760, doi:10.1126/science.1252229.Viruses are the most abundant biological entities in the oceans and a pervasive cause of mortality of microorganisms that drive biogeochemical cycles. Although the ecological and evolutionary impacts of viruses on marine phototrophs are well-recognized, little is known about their impact on ubiquitous marine lithotrophs. Here we report 18 genome sequences of double-stranded DNA viruses that putatively infect widespread sulfur-oxidizing bacteria. Fifteen of these viral genomes contain auxiliary metabolic genes for the alpha and gamma subunits of reverse dissimilatory sulfite reductase (rdsr). This enzyme oxidizes elemental sulfur, which is abundant in the hydrothermal plumes studied here. Our findings implicate viruses as a key agent in the sulfur cycle and as a reservoir of genetic diversity for bacterial enzymes that underpin chemosynthesis in the deep oceans.This project is funded in part by the Gordon and Betty Moore Foundation Grant GBMF2609 and National Science Foundation Grant OCE1038006

Niche differentiation of sulfur-oxidizing bacteria (SUP05) in submarine hydrothermal plumes

Hydrothermal plumes transport reduced chemical species and metals into the open ocean. Despite their considerable spatial scale and impact on biogeochemical cycles, niche differentiation of abundant microbial clades is poorly understood. Here, we analyzed the microbial ecology of two bathy- (Brothers volcano; BrV-cone and northwest caldera; NWC) and a mesopelagic (Macauley volcano; McV) plumes on the Kermadec intra-oceanic arc in the South Pacific Ocean. The microbial community structure, determined by a combination of 16S rRNA gene, fluorescence in situ hybridization and metagenome analysis, was similar to the communities observed in other sulfur-rich plumes. This includes a dominance of the vent characteristic SUP05 clade (up to 22% in McV and 51% in BrV). In each of the three plumes analyzed, the community was dominated by a different yet uncultivated chemoautotrophic SUP05 species, here, provisionally named, Candidatus Thioglobus vadi (McV), Candidatus Thioglobus vulcanius (BrV-cone) and Candidatus Thioglobus plumae (BrV-NWC). Statistical analyses, genomic potential and mRNA expression profiles suggested a SUP05 niche partitioning based on sulfide and iron concentration as well as water depth. A fourth SUP05 species was present at low frequency throughout investigated plume samples and may be capable of heterotrophic or mixotrophic growth. Taken together, we propose that small variations in environmental parameters and depth drive SUP05 niche partitioning in hydrothermal plumes

Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Environmental Microbiology 20 (2018): 769–784, doi:10.1111/1462-2920.14011.At deep-sea hydrothermal vents, microbial communities thrive across geochemical gradients above, at, and below the seafloor. In this study, we determined the gene content and transcription patterns of microbial communities and specific populations to understand the taxonomy and metabolism both spatially and temporally across geochemically different diffuse fluid hydrothermal vents. Vent fluids were examined via metagenomic, metatranscriptomic, genomic binning, and geochemical analyses from Axial Seamount, an active submarine volcano on the Juan de Fuca Ridge in the NE Pacific Ocean, from 2013 to 2015 at three different vents: Anemone, Marker 33, and Marker 113. Results showed that individual vent sites maintained microbial communities and specific populations over time, but with spatially distinct taxonomic, metabolic potential, and gene transcription profiles. The geochemistry and physical structure of each vent both played important roles in shaping the dominant organisms and metabolisms present at each site. Genomic binning identified key populations of SUP05, Aquificales and methanogenic archaea carrying out important transformations of carbon, sulfur, hydrogen, and nitrogen, with groups that appear unique to individual sites. This work highlights the connection between microbial metabolic processes, fluid chemistry, and microbial population dynamics at and below the seafloor and increases understanding of the role of hydrothermal vent microbial communities in deep ocean biogeochemical cycles.Gordon and Betty Moore Foundation Grant Number: GBMF3297; NSF Center for Dark Energy Biosphere Investigations Grant Number: OCE—0939564; Schmidt Ocean Institut

The unique chemistry of Eastern Mediterranean water masses selects for distinct microbial communities by depth

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Nano-Sized and Filterable Bacteria and Archaea:Biodiversity and Function

Nano-sized and filterable microorganisms are thought to represent the smallest living organisms on earth and are characterized by their small size (50–400 nm) and their ability to physically pass through &lt;0.45 μm pore size filters. They appear to be ubiquitous in the biosphere and are present at high abundance across a diverse range of habitats including oceans, rivers, soils, and subterranean bedrock. Small-sized organisms are detected by culture-independent and culture-dependent approaches, with most remaining uncultured and uncharacterized at both metabolic and taxonomic levels. Consequently, their significance in ecological roles remain largely unknown. Successful isolation, however, has been achieved for some species (e.g., Nanoarchaeum equitans and “Candidatus Pelagibacter ubique”). In many instances, small-sized organisms exhibit a significant genome reduction and loss of essential metabolic pathways required for a free-living lifestyle, making their survival reliant on other microbial community members. In these cases, the nano-sized prokaryotes can only be co-cultured with their ‘hosts.’ This paper analyses the recent data on small-sized microorganisms in the context of their taxonomic diversity and potential functions in the environment

Evidence for hydrogen oxidation and metabolic plasticity in widespread deep-sea sulfur-oxidizing bacteria

Author Posting. © The Author(s), 2012. This is the author's version of the work. It is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences of the United States of America 110 (2013): 330-335, doi:10.1073/pnas.1215340110.Hydrothermal vents are a well-known source of energy that powers chemosynthesis in the deep sea. Recent work suggests that microbial chemosynthesis is also surprisingly pervasive throughout the dark oceans, serving as a significant CO2 sink even at sites far-removed from vents. Ammonia and sulfur have been identified as potential electron donors for this chemosynthesis, but they do not fully account for measured rates of dark primary production in the pelagic water column. Here we use metagenomic and metatranscriptomic analyses to show that deep-sea populations of the SUP05 group of uncultured sulfur oxidizing Gammaproteobacteria, which are abundant in widespread and diverse marine environments, contain and highly express genes encoding group 1 Ni-Fe hydrogenase enzymes for H2 oxidation. Reconstruction of near-complete genomes of two co-occurring SUP05 populations in hydrothermal plumes and deep waters of the Gulf of California enabled detailed population-specific metatranscriptomic analyses, revealing dynamic patterns of gene content and transcript abundance. SUP05 transcripts for genes involved in H2 and sulfur oxidation are most abundant in hydrothermal plumes where these electron donors are enriched. In contrast, a second hydrogenase has more abundant transcripts in background deep sea samples. Coupled with results from a bioenergetic model that suggest that H2 oxidation can contribute significantly to the SUP05 energy budget, these findings reveal the potential importance of H2 as a key energy source in the deep ocean. This study also highlights the genomic plasticity of SUP05, which enables this widely distributed group to optimize its energy metabolism (electron donor and acceptor) to local geochemical conditions.This project is funded in part by the Gordon and Betty Moore Foundation and the National Science Foundation (OCE 1029242)

Capacity of deep‐sea corals to obtain nutrition from cold seeps aligned with microbiome reorganization

Cold seeps in the deep sea harbor various animals that have adapted to utilize seepage chemicals with the aid of chemosynthetic microbes that serve as primary producers. Corals are among the animals that live near seep habitats and yet, there is a lack of evidence that corals gain benefits and/or incur costs from cold seeps. Here, we focused on Callogorgia delta and Paramuricea sp. type B3 that live near and far from visual signs of currently active seepage at five sites in the deep Gulf of Mexico. We tested whether these corals rely on chemosynthetically-derived food in seep habitats and how the proximity to cold seeps may influence; (i) coral colony traits (i.e., health status, growth rate, regrowth after sampling, and branch loss) and associated epifauna, (ii) associated microbiome, and (iii) host transcriptomes. Stable isotope data showed that many coral colonies utilized chemosynthetically derived food, but the feeding strategy differed by coral species. The microbiome composition of C. delta, unlike Paramuricea sp., varied significantly between seep and non-seep colonies and both coral species were associated with various sulfur-oxidizing bacteria (SUP05). Interestingly, the relative abundances of SUP05 varied among seep and non-seep colonies and were strongly correlated with carbon and nitrogen stable isotope values. In contrast, the proximity to cold seeps did not have a measurable effect on gene expression, colony traits, or associated epifauna in coral species. Our work provides the first evidence that some corals may gain benefits from living near cold seeps with apparently limited costs to the colonies. Cold seeps provide not only hard substrate but also food to cold-water corals. Furthermore, restructuring of the microbiome communities (particularly SUP05) is likely the key adaptive process to aid corals in utilizing seepage-derived carbon. This highlights that those deep-sea corals may upregulate particular microbial symbiont communities to cope with environmental gradients

Bacterial niche adaptation at hydrothermal vents

At deep sea hydrothermal fields, a mixing gradient between hot reduced fluids and cold oxygenated sea water creates a number of micro-environments with different physico-chemical conditions in direct proximity to each other. Although many of the key microorganisms in these environments have been identified and described, a systematic understanding of their distribution across the mixing gradient and their niche partitioning is still missing. In my doctoral thesis, I investigated the interplay of geochemical settings, microbial community structures, and diversification of microorganisms in three collaborative studies of hydrothermal vent fields in the Atlantic and Pacific Oceans. Taken together, this thesis provides a detailed overview of the microbial community structures in hydrothermal vents. It deepens our understanding of niche differentiation of major marine sulfur oxidizers, and offers valuable insights into microbial diversification