Spatially resolved sampling reveals dynamic microbial communities in rising hydrothermal plumes across a back-arc basin.
ABSTRACT: Within hydrothermal plumes, chemosynthetic processes and microbe-mineral interactions drive primary productivity in deep-ocean food webs and may influence transport of elements such as iron. However, the source of microorganisms in plumes and the factors governing how these communities assemble are poorly understood, in part due to lack of data from early stages of plume formation. In this study, we examined microbial community composition of rising hydrothermal plumes from five vent fields along the Eastern Lau Spreading Center. Seafloor and plume microbial communities were significantly dissimilar and shared few phylotypes. Plume communities were highly similar to each other with significant differences in community membership only between Kilo Moana and Mariner, two vents that are separated by extremes in depth, latitude and geochemistry. Systematic sampling of waters surrounding the vents revealed that species richness and phylogenetic diversity was typically highest near the vent orifice, implying mixing of microbial communities from the surrounding habitats. Above-plume background communities were primarily dominated by SAR11, SAR324 and MG-I Archaea, while SUP05, Sulfurovum, Sulfurimonas, SAR324 and Alteromonas were abundant in plume and near-bottom background communities. These results show that the ubiquitous water-column microorganisms populate plume communities, and that the composition of background seawater exerts primary influence on plume community composition, with secondary influence from geochemical and/or physical properties of vents. Many of these pervasive deep-ocean organisms are capable of lithotrophy, suggesting that they are poised to use inorganic electron donors encountered in hydrothermal plumes.
Project description:Hydrothermal plumes are an important yet understudied component of deep-sea vent microbial ecosystems. The significance of plume microbial processes can be appreciated from three perspectives: (1) mediation of plume biogeochemistry, (2) dispersal of seafloor hydrothermal vent microbes between vents sites, (3) as natural laboratories for understanding the ecology, physiology, and function of microbial groups that are distributed throughout the pelagic deep sea. Plume microbiology has been largely neglected in recent years, especially relative to the extensive research conducted on seafloor and subseafloor systems. Rapidly advancing technologies for investigating microbial communities provide new motivation and opportunities to characterize this important microbial habitat. Here we briefly highlight microbial contributions to plume and broader ocean (bio)geochemistry and review recent work to illustrate the ecological and biogeographic linkages between plumes, seafloor vent habitats, and other marine habitats such as oxygen minimum zones (OMZs), cold seeps, and oil spills. 16S rRNA gene surveys and metagenomic/-transcriptomic data from plumes point to dominant microbial populations, genes, and functions that are also operative in OMZs (SUP05, ammonia-oxidizing Archaea, and SAR324 Deltaproteobacteria) and hydrocarbon-rich environments (methanotrophs). Plume microbial communities are distinct from those on the seafloor or in the subsurface but contain some signatures of these habitats, consistent with the notion that plumes are potential vectors for dispersal of microorganisms between seafloor vent sites. Finally, we put forward three pressing questions for the future of deep-sea hydrothermal plume research and consider interactions between vents and oceans on global scales.
Project description:Microorganisms mediate geochemical processes in deep-sea hydrothermal vent plumes, which are a conduit for transfer of elements and energy from the subsurface to the oceans. Despite this important microbial influence on marine geochemistry, the ecology and activity of microbial communities in hydrothermal plumes is largely unexplored. Here, we use a coordinated metagenomic and metatranscriptomic approach to compare microbial communities in Guaymas Basin hydrothermal plumes to background waters above the plume and in the adjacent Carmen Basin. Despite marked increases in plume total RNA concentrations (3-4 times) and microbially mediated manganese oxidation rates (15-125 times), plume and background metatranscriptomes were dominated by the same groups of methanotrophs and chemolithoautotrophs. Abundant community members of Guaymas Basin seafloor environments (hydrothermal sediments and chimneys) were not prevalent in the plume metatranscriptome. De novo metagenomic assembly was used to reconstruct genomes of abundant populations, including Marine Group I archaea, Methylococcaceae, SAR324 Deltaproteobacteria and SUP05 Gammaproteobacteria. Mapping transcripts to these genomes revealed abundant expression of genes involved in the chemolithotrophic oxidation of ammonia (amo), methane (pmo) and sulfur (sox). Whereas amo and pmo gene transcripts were abundant in both plume and background, transcripts of sox genes for sulfur oxidation from SUP05 groups displayed a 10-20-fold increase in plumes. We conclude that the biogeochemistry of Guaymas Basin hydrothermal plumes is mediated by microorganisms that are derived from seawater rather than from seafloor hydrothermal environments such as chimneys or sediments, and that hydrothermal inputs serve as important electron donors for primary production in the deep Gulf of California.
Project description:To determine microbial community composition, community spatial structure and possible key microbial processes in the shallow-sea hydrothermal vent systems off NE Taiwan's coast, we examined the bacterial and archaeal communities of four samples collected from the water column extending over a redoxocline gradient of a yellow and four from a white hydrothermal vent. Ribosomal tag pyrosequencing based on DNA and RNA showed statistically significant differences between the bacterial and archaeal communities of the different hydrothermal plumes. The bacterial and archaeal communities from the white hydrothermal plume were dominated by sulfur-reducing Nautilia and Thermococcus, whereas the yellow hydrothermal plume and the surface water were dominated by sulfide-oxidizing Thiomicrospira and Euryarchaeota Marine Group II, respectively. Canonical correspondence analyses indicate that methane (CH(4)) concentration was the only statistically significant variable that explains all community cluster patterns. However, the results of pyrosequencing showed an essential absence of methanogens and methanotrophs at the two vent fields, suggesting that CH(4) was less tied to microbial processes in this shallow-sea hydrothermal system. We speculated that mixing between hydrothermal fluids and the sea or meteoric water leads to distinctly different CH(4) concentrations and redox niches between the yellow and white vents, consequently influencing the distribution patterns of the free-living Bacteria and Archaea. We concluded that sulfur-reducing and sulfide-oxidizing chemolithoautotrophs accounted for most of the primary biomass synthesis and that microbial sulfur metabolism fueled microbial energy flow and element cycling in the shallow hydrothermal systems off the coast of NE Taiwan.
Project description:There are still notable gaps regarding the detailed distribution of microorganisms between and within insular habitats such as deep-sea hydrothermal vents. This study investigates the community composition of black smoker vent microorganisms in the Southern Hemisphere, and changes thereof along a spatial and chemical gradient ranging from the vent plume to surrounding waters. We sampled two hydrothermal vent fields, one at the South West Indian Ridge (SWIR), the other at the East Scotia Ridge (ESR). Samples were collected across vent fields at varying vertical distances from the origin of the plumes. The microbial data were sequenced on an Illumina MiSeq platform for the 16SrRNA gene. A substantial amount of vent-specific putative chemosynthetic microorganisms were found, particularly in samples from focused hydrothermal venting. Common vent-specific organisms from both vent fields were the genera Arcobacter, Caminibacter and Sulfurimonas from the Epsilonproteobacteria and the SUP05 group from the Gammaproteobacteria. There were no major differences in microbial composition between SWIR and ESR for focused plume samples. However, within the ESR the diffuse flow and focused samples differed significantly in microbial community composition and relative abundance. For Epsilonproteobacteria, we found evidence of niche-specificity to hydrothermal vent environments. This taxon decreased in abundance by three orders of magnitude from the vent orifice to background water. Epsilonproteobacteria distribution followed a distance-decay relationship as vent-effluents mixed with the surrounding seawater. This study demonstrates strong habitat affinity of vent microorganisms on a metre scale with distinct environmental selection.
Project description:Submarine hydrothermal vents perturb the deep-ocean microbiome by injecting reduced chemical species into the water column that act as an energy source for chemosynthetic organisms. These systems thus provide excellent natural laboratories for studying the response of microbial communities to shifts in marine geochemistry. The present study explores the processes that regulate coupled microbial-geochemical dynamics in hydrothermal plumes by means of a novel mathematical model, which combines thermodynamics, growth and reaction kinetics, and transport processes derived from a fluid dynamics model. Simulations of a plume located in the ABE vent field of the Lau basin were able to reproduce metagenomic observations well and demonstrated that the magnitude of primary production and rate of autotrophic growth are largely regulated by the energetics of metabolisms and the availability of electron donors, as opposed to kinetic parameters. Ambient seawater was the dominant source of microbes to the plume and sulphur oxidisers constituted almost 90% of the modelled community in the neutrally-buoyant plume. Data from drifters deployed in the region allowed the different time scales of metabolisms to be cast in a spatial context, which demonstrated spatial succession in the microbial community. While growth was shown to occur over distances of tens of kilometers, microbes persisted over hundreds of kilometers. Given that high-temperature hydrothermal systems are found less than 100 km apart on average, plumes may act as important vectors between different vent fields and other environments that are hospitable to similar organisms, such as oil spills and oxygen minimum zones.
Project description:Microbial chemosynthesis within deep-sea hydrothermal vent plumes is a regionally important source of organic carbon to the deep ocean. Although chemolithoautotrophs within hydrothermal plumes have attracted much attention, a gap remains in understanding the fate of organic carbon produced via chemosynthesis. In the present study, we conducted shotgun metagenomic and metatranscriptomic sequencing on samples from deep-sea hydrothermal vent plumes and surrounding background seawaters at Guaymas Basin (GB) in the Gulf of California. De novo assembly of metagenomic reads and binning by tetranucleotide signatures using emergent self-organizing maps (ESOM) revealed 66 partial and nearly complete bacterial genomes. These bacterial genomes belong to 10 different phyla: Actinobacteria, Bacteroidetes, Chloroflexi, Deferribacteres, Firmicutes, Gemmatimonadetes, Nitrospirae, Planctomycetes, Proteobacteria, Verrucomicrobia. Although several major transcriptionally active bacterial groups (Methylococcaceae, Methylomicrobium, SUP05, and SAR324) displayed methanotrophic and chemolithoautotrophic metabolisms, most other bacterial groups contain genes encoding extracellular peptidases and carbohydrate metabolizing enzymes with significantly higher transcripts in the plume than in background, indicating they are involved in degrading organic carbon derived from hydrothermal chemosynthesis. Among the most abundant and active heterotrophic bacteria in deep-sea hydrothermal plumes are Planctomycetes, which accounted for seven genomes with distinct functional and transcriptional activities. The Gemmatimonadetes and Verrucomicrobia also had abundant transcripts involved in organic carbon utilization. These results extend our knowledge of heterotrophic metabolism of bacterial communities in deep-sea hydrothermal plumes.
Project description:Faunal assemblages at hydrothermal vents associated with island-arc volcanism are less well known than those at vents on mid-ocean ridges and back-arc spreading centres. This study characterizes chemosynthetic biotopes at active hydrothermal vents discovered at the Kemp Caldera in the South Sandwich Arc. The caldera hosts sulfur and anhydrite vent chimneys in 1375-1487 m depth, which emit sulfide-rich fluids with temperatures up to 212°C, and the microbial community of water samples in the buoyant plume rising from the vents was dominated by sulfur-oxidizing Gammaproteobacteria. A total of 12 macro- and megafaunal taxa depending on hydrothermal activity were collected in these biotopes, of which seven species were known from the East Scotia Ridge (ESR) vents and three species from vents outside the Southern Ocean. Faunal assemblages were dominated by large vesicomyid clams, actinostolid anemones, Sericosura sea spiders and lepetodrilid and cocculinid limpets, but several taxa abundant at nearby ESR hydrothermal vents were rare such as the stalked barnacle Neolepas scotiaensis. Multivariate analysis of fauna at Kemp Caldera and vents in neighbouring areas indicated that the Kemp Caldera is most similar to vent fields in the previously established Southern Ocean vent biogeographic province, showing that the species composition at island-arc hydrothermal vents can be distinct from nearby seafloor-spreading systems. ? 13C and ? 15N isotope values of megafaunal species analysed from the Kemp Caldera were similar to those of the same or related species at other vent fields, but none of the fauna sampled at Kemp Caldera had ? 13C values, indicating nutritional dependence on Epsilonproteobacteria, unlike fauna at other island-arc hydrothermal vents.
Project description:Deep-sea hydrothermal vents are a significant source of dissolved metals to the global oceans, producing midwater plumes enriched in metals that are transported thousands of kilometers from the vent source. Particle precipitation upon emission of hydrothermal fluids controls metal speciation and the magnitude of metal export. Here, we document metal sulfide particles, including pyrite nanoparticles, within the first meter of buoyant plumes from three high-temperature vents at the East Pacific Rise. We observe a zone of particle settling 10-20 cm from the orifice, indicated by stable sulfur isotopes; however, we also demonstrate that nanoparticulate pyrite (FeS2) is not removed from the plume and can account for over half of the filtered Fe (≤0.2 µm) up to one meter from the vent orifice. The persistence of nanoparticulate pyrite demonstrates that it is an important mechanism for near-vent Fe stabilisation and highlights the potential role of nanoparticles in element transport.
Project description:Viruses are ubiquitous in the oceans and critical components of marine microbial communities, regulating nutrient transfer to higher trophic levels or to the dissolved organic pool through lysis of host cells. Hydrothermal vent systems are oases of biological activity in the deep oceans, for which knowledge of biodiversity and its impact on global ocean biogeochemical cycling is still in its infancy. In order to gain biological insight into viral communities present in hydrothermal vent systems, we developed a method based on deep-sequencing of pulsed field gel electrophoretic bands representing key viral fractions present in seawater within and surrounding a hydrothermal plume derived from Loki's Castle vent field at the Arctic Mid-Ocean Ridge. The reduction in virus community complexity afforded by this novel approach enabled the near-complete reconstruction of a lambda-like phage genome from the virus fraction of the plume. Phylogenetic examination of distinct gene regions in this lambdoid phage genome unveiled diversity at loci encoding superinfection exclusion- and integrase-like proteins. This suggests the importance of fine-tuning lyosgenic conversion as a viral survival strategy, and provides insights into the nature of host-virus and virus-virus interactions, within hydrothermal plumes. By reducing the complexity of the viral community through targeted sequencing of prominent dsDNA viral fractions, this method has selectively mimicked virus dominance approaching that hitherto achieved only through culturing, thus enabling bioinformatic analysis to locate a lambdoid viral "needle" within the greater viral community "haystack". Such targeted analyses have great potential for accelerating the extraction of biological knowledge from diverse and poorly understood environmental viral communities.
Project description:The abundance, diversity, activity, and composition of microbial communities in sulfide structures both of active and inactive vents were investigated by culture-independent methods. These sulfide structures were collected at four hydrothermal fields, both on- and off-axis of the back-arc spreading center of the Southern Mariana Trough. The microbial abundance and activity in the samples were determined by analyzing total organic content, enzymatic activity, and copy number of the 16S rRNA gene. To assess the diversity and composition of the microbial communities, 16S rRNA gene clone libraries including bacterial and archaeal phylotypes were constructed from the sulfide structures. Despite the differences in the geological settings among the sampling points, phylotypes related to the Epsilonproteobacteria and cultured hyperthermophilic archaea were abundant in the libraries from the samples of active vents. In contrast, the relative abundance of these phylotypes was extremely low in the libraries from the samples of inactive vents. These results suggest that the composition of microbial communities within sulfide structures dramatically changes depending on the degree of hydrothermal activity, which was supported by statistical analyses. Comparative analyses suggest that the abundance, activity and diversity of microbial communities within sulfide structures of inactive vents are likely to be comparable to or higher than those in active vent structures, even though the microbial community composition is different between these two types of vents. The microbial community compositions in the sulfide structures of inactive vents were similar to those in seafloor basaltic rocks rather than those in marine sediments or the sulfide structures of active vents, suggesting that the microbial community compositions on the seafloor may be constrained by the available energy sources. Our findings provide helpful information for understanding the biogeography, biodiversity and microbial ecosystems in marine environments.