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"Hydrothermal vent ecology."
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Virus diversity and interactions with hosts in deep-sea hydrothermal vents
Background
The deep sea harbors many viruses, yet their diversity and interactions with hosts in hydrothermal ecosystems are largely unknown. Here, we analyzed the viral composition, distribution, host preference, and metabolic potential in different habitats of global hydrothermal vents, including vent plumes, background seawater, diffuse fluids, and sediments.
Results
From 34 samples collected at eight vent sites, a total of 4662 viral populations (vOTUs) were recovered from the metagenome assemblies, encompassing diverse phylogenetic groups and defining many novel lineages. Apart from the abundant unclassified viruses, tailed phages are most predominant across the global hydrothermal vents, while single-stranded DNA viruses, including Microviridae and small eukaryotic viruses, also constitute a significant part of the viromes. As revealed by protein-sharing network analysis, hydrothermal vent viruses formed many novel genus-level viral clusters and are highly endemic to specific vent sites and habitat types. Only 11% of the vOTUs can be linked to hosts, which are the key microbial taxa of hydrothermal habitats, such as
Gammaproteobacteria
and
Campylobacterota
. Intriguingly, vent viromes share some common metabolic features in that they encode auxiliary genes that are extensively involved in the metabolism of carbohydrates, amino acids, cofactors, and vitamins. Specifically, in plume viruses, various auxiliary genes related to methane, nitrogen, and sulfur metabolism were observed, indicating their contribution to host energy conservation. Moreover, the prevalence of sulfur-relay pathway genes indicated the significant role of vent viruses in stabilizing the tRNA structure, which promotes host adaptation to steep environmental gradients.
Conclusions
The deep-sea hydrothermal systems hold untapped viral diversity with novelty. They may affect both vent prokaryotic and eukaryotic communities and modulate host metabolism related to vent adaptability. More explorations are needed to depict global vent virus diversity and its roles in this unique ecosystem.
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Video Abstract
Journal Article
Host–Endosymbiont Genome Integration in a Deep-Sea Chemosymbiotic Clam
Endosymbiosis with chemosynthetic bacteria has enabled many deep-sea invertebrates to thrive at hydrothermal vents and cold seeps, but most previous studies on this mutualism have focused on the bacteria only. Vesicomyid clams dominate global deep-sea chemosynthesis-based ecosystems. They differ from most deep-sea symbiotic animals in passing their symbionts from parent to offspring, enabling intricate coevolution between the host and the symbiont. Here, we sequenced the genomes of the clam Archivesica marissinica (Bivalvia: Vesicomyidae) and its bacterial symbiont to understand the genomic/metabolic integration behind this symbiosis. At 1.52 Gb, the clam genome encodes 28 genes horizontally transferred from bacteria, a large number of pseudogenes and transposable elements whose massive expansion corresponded to the timing of the rise and subsequent divergence of symbiont-bearing vesicomyids. The genome exhibits gene family expansion in cellular processes that likely facilitate chemoautotrophy, including gas delivery to support energy and carbon production, metabolite exchange with the symbiont, and regulation of the bacteriocyte population. Contraction in cellulase genes is likely adaptive to the shift from phytoplankton-derived to bacteria-based food. It also shows contraction in bacterial recognition gene families, indicative of suppressed immune response to the endosymbiont. The gammaproteobacterium endosymbiont has a reduced genome of 1.03 Mb but retains complete pathways for sulfur oxidation, carbon fixation, and biosynthesis of 20 common amino acids, indicating the host’s high dependence on the symbiont for nutrition. Overall, the host–symbiont genomes show not only tight metabolic complementarity but also distinct signatures of coevolution allowing the vesicomyids to thrive in chemosynthesis-based ecosystems.
Journal Article
Contrasted phylogeographic patterns of hydrothermal vent gastropods along South West Pacific : Woodlark Basin, a possible contact zone and/or stepping-stone
Compares phylogeographic patterns of several vent gastropods across South West Pacific back-arc basins and the newly-discovered La Scala site on the Woodlark Ridge by analysing their genetic divergence using a barcoding approach. Focuses on six genera of vent gastropods widely distributed in the region : Lepetodrilus, Symmetromphalus, Lamellomphalus, Shinkailepas, Desbruyeresia, and Provanna Source: National Library of New Zealand Te Puna Matauranga o Aotearoa, licensed by the Department of Internal Affairs for re-use under the Creative Commons Attribution 3.0 New Zealand Licence.
Journal Article
Global patterns of diversity and metabolism of microbial communities in deep-sea hydrothermal vent deposits
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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Video Abstract
Journal Article
Characterization of an undocumented CO.sub.2 hydrothermal vent system in the Mediterranean Sea: Implications for ocean acidification forecasting
A previously undocumented shallow water hydrothermal field from Sicily (Southern Tyrrhenian Sea, Italy) is here described, based on a multidisciplinary investigation. The field, covering an area of nearly 8000 m.sup.2 and a depth from the surface to -5 m, was explored in June 2021 to characterise the main physico-chemical features of the water column, describe the bottom topography and features, and identify the main megabenthic and nektonic species. Twenty sites were investigated to characterise the carbonate system. Values of pH ranged between 7.84 and 8.04, [OMEGA]Ca between 3.68 and 5.24 and [OMEGA]Ar from 2.41 to 3.44. Geochemical analyses of hydrothermal gases revealed a dominance of CO.sub.2 (98.1%) together with small amounts of oxygen and reactive gases. Helium isotope ratios (R/Ra = 2.51) and [delta].sup.13 C.sub.CO2 suggest an inorganic origin of hydrothermal degassing of CO.sub.2 and the ascent of heat and deep-seated magmatic fluids to the surface. Visual census of fishes and megabenthos (mainly sessile organisms) allowed the identification of 64 species, four of which are protected by the SPA/BIO Protocol and two by the International Union for Conservation of Nature. The macroalgae Halopteris scoparia and Jania rubens and the sponge Sarcotragus sp. were the dominant taxa in the area, while among fishes Coris julis and Chromis chromis were the most abundant species. This preliminary investigation of San Giorgio vent field suggests that the site could be of interest and suitable for future experimental studies of ocean acidification.
Journal Article
Organic iron-binding ligands mediate dissolved-particulate exchange in hydrothermal vent plumes along the Mid-Atlantic Ridge
Hydrothermal vents are important contributors to the dissolved iron (Fe) inventory in the ocean. Investigating the processes underlying Fe behavior in hydrothermal plumes is challenging, but important for constraining deep ocean Fe cycling. Field studies suggest that the retention of hydrothermal Fe in the deep ocean is primarily supported by two mechanisms: the formation of colloidal nanoparticles and the stabilization of Fe by organic ligands. Here we present a novel dataset from shipboard incubation experiments designed to investigate the interplay between these two processes and how they contribute to the stabilization of Fe away from ridge axes. Filtered and unfiltered water collected from the hydrothermal plumes of three vent fields along the Mid-Atlantic Ridge as part of GEOTRACES cruise GA13 was incubated in the dark and regularly sampled over time (up to 3 weeks) for concentrations of size-fractionated Fe and Fe-binding ligands, for dissolved Fe isotopic composition, and for microbial community composition. We observed rapid exchange of Fe between physicochemical phases that appeared to be mediated in part by organic Fe-binding ligands at each stage of plume evolution. Weaker Fe-binding ligands sources from the vents were largely lost to the particulate phase with colloidal Fe phases via aggregation early in plume development, similar to the loss of Fe and organic matter commonly observed in estuarine systems. Soluble organic ligand production was observed in later stages of all unfiltered incubations followed by mobilization of particulate and colloidal Fe into the soluble phase in the longer incubations, revealing a potentially important mechanism for generating the persistent Fe observed in long-range plumes.
Journal Article
Differential feeding habits of the shallow-water hydrothermal vent crab Xenograpsus testudinatus correlate with their resident vent types at a scale of meters
The shallow-water hydrothermal vents (SVs) located off Kueishan (KS) Island, Taiwan, are one of the world's most intensively studied vent systems. It has long been known that white vents (WVs) and yellow vents (YVs) differ in the color and composition of the vent plumes. The endemic vent crabs (Xenograpsus testudinatus) are abundant in both vent types, and ovigerous females migrate to the vent periphery with a distance of 100–200 m to release their offspring. However, most research on the vent crabs was associated with WV or unspecified vent areas. To increase our knowledge of the crabs dwelling in other vent types, we compared the feeding habits of the vent crabs living in WV and YV with 2 sampling months. Specifically, we examined the benthic community of WV and YV, the isotopic niche width, and protein expression patterns of the crabs from the two vents at a distance of 100 m and sampled in July and August 2010. The coverage of sessile organisms and low-mobility fauna in WV was more abundant than in YV, based on the survey in August 2010. The δ13C and δ15N values of crabs differed spatially and temporally (multivariate analysis of variance test; p<0.05). The niche width of the vent crabs from YV-August (0.88 ‰2) narrowed substantially compared to the rest, i.e., YV-July (2.94 ‰2), WV-July (2.88 ‰2), and WV-August (3.62 ‰2; p<0.05), respectively. Based on the protein expression patterns, the vent crabs exhibited three groups, i.e., WV-July and YV-July, WV-August, and YV-August, respectively. Our results indicated that the dwelling crabs were associated with their living vent, and within-vent variability was more noticeable in YV compared to WV. We suggested that vent crabs inhabit their resident vent. Even at a scale of meters, trans-vent movement is probably rare as an adaptation to minimize predation risk.
Journal Article
Microbial succession during the transition from active to inactive stages of deep-sea hydrothermal vent sulfide chimneys
Background
Deep-sea hydrothermal vents are highly productive biodiversity hotspots in the deep ocean supported by chemosynthetic microorganisms. Prominent features of these systems are sulfide chimneys emanating high-temperature hydrothermal fluids. While several studies have investigated the microbial diversity in both active and inactive sulfide chimneys that have been extinct for up to thousands of years, little is known about chimneys that have ceased activity more recently, as well as the microbial succession occurring during the transition from active to inactive chimneys.
Results
Genome-resolved metagenomics was applied to an active and a recently extinct (~ 7 years) sulfide chimney from the 9–10° N hydrothermal vent field on the East Pacific Rise. Full-length 16S rRNA gene and a total of 173 high-quality metagenome assembled genomes (MAGs) were retrieved for comparative analysis. In the active chimney (L-vent), sulfide- and/or hydrogen-oxidizing
Campylobacteria
and
Aquificae
with the potential for denitrification were identified as the dominant community members and primary producers, fixing carbon through the reductive tricarboxylic acid (rTCA) cycle. In contrast, the microbiome of the recently extinct chimney (M-vent) was largely composed of heterotrophs from various bacterial phyla, including
Delta
-/
Beta
-/
Alphaproteobacteria
and
Bacteroidetes
.
Gammaproteobacteria
were identified as the main primary producers, using the oxidation of metal sulfides and/or iron oxidation coupled to nitrate reduction to fix carbon through the Calvin-Benson-Bassham (CBB) cycle. Further analysis revealed a phylogenetically distinct
Nitrospirae
cluster that has the potential to oxidize sulfide minerals coupled to oxygen and/or nitrite reduction, as well as for sulfate reduction, and that might serve as an indicator for the early stages of chimneys after venting has ceased.
Conclusions
This study sheds light on the composition, metabolic functions, and succession of microbial communities inhabiting deep-sea hydrothermal vent sulfide chimneys. Collectively, microbial succession during the life span of a chimney could be described to proceed from a “fluid-shaped” microbial community in newly formed and actively venting chimneys supported by the oxidation of reductants in the hydrothermal fluid to a “mineral-shaped” community supported by the oxidation of minerals after hydrothermal activity has ceased. Remarkably, the transition appears to occur within the first few years, after which the communities stay stable for thousands of years.
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Video Abstract
Journal Article
Beta diversity differs among hydrothermal vent systems: Implications for conservation
Deep-sea hydrothermal vent habitats are small, rare and support unique species through chemosynthesis. As this vulnerable ecosystem is increasingly threatened by human activities, management approaches should address biodiversity conservation. Diversity distribution data provide a useful basis for management approaches as patterns of β-diversity (the change in diversity from site to site) can guide conservation decisions. Our question is whether such patterns are similar enough across vent systems to support a conservation strategy that can be deployed regardless of location. We compile macrofaunal species occurrence data for vent systems in three geological settings in the North Pacific: volcanic arc, back-arc and mid-ocean ridge. Recent discoveries in the Mariana region provide the opportunity to characterize diversity at many vent sites. We examine the extent to which diversity distribution patterns differ among the systems by comparing pairwise β-diversity, nestedness and their additive components. A null model approach that tests whether species compositions of each site pair are more or less similar than random provides insight into community assembly processes. We resolve several taxonomic uncertainties and find that the Mariana arc and back-arc share only 8% of species despite their proximity. Species overlap, species replacement and richness differences create different diversity distributions within the three vent systems; the arc system exhibits much greater β-diversity than both the back-arc and mid-ocean ridge systems which, instead, show greater nestedness. The influence of nestedness on β-diversity also increased from the arc to back-arc to ridge. Community assembly processes appear more deterministic in the arc and ridge systems while back-arc site pairs deviate little from the null expectation. These analyses reflect the need for a variety of management strategies that consider the character of diversity distribution to protect hydrothermal vents, especially in the context of mining hydrothermal deposits.
Journal Article