Studies of deeply buried, sedimentary microbial communities and associated biogeochemical processes during Ocean Drilling Program Leg 201 showed elevated prokaryotic cell numbers in sediment layers where methane is consumed anaerobically at the expense of sulfate. Here, we show that extractable archaeal rRNA, selecting only for active community members in these ecosystems, is dominated by sequences of uncultivated Archaea affiliated with the Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group, whereas known methanotrophic Archaea are not detectable. Carbon flow reconstructions based on stable isotopic compositions of whole archaeal cells, intact archaeal membrane lipids, and other sedimentary carbon pools indicate that these Archaea assimilate sedimentary organic compounds other than methane even though methanotrophy accounts for a major fraction of carbon cycled in these ecosystems. Oxidation of methane by members of Marine Benthic Group B and the Miscellaneous Crenarchaeotal Group without assimilation of methane-carbon provides a plausible explanation. Maintenance energies of these subsurface communities appear to be orders of magnitude lower than minimum values known from laboratory observations, and ecosystem-level carbon budgets suggest that community turnover times are on the order of 100 -2,000 years. Our study provides clues about the metabolic functionality of two cosmopolitan groups of uncultured Archaea.anaerobic methanotrophy ͉ deep biosphere ͉ FISH-secondary ion MS ͉ intact polar lipids ͉ stable carbon isotopes
Metagenomic analyses of viruses have revealed widespread diversity in the viriosphere, but it remains a challenge to identify specific hosts for a viral assemblage. To address this problem, we analyze the viral metagenome of a northeast Pacific hydrothermal vent with a comprehensive database of spacers derived from the clustered regularly interspaced short palindromic repeat (CRISPR) putative immune system. CRISPR spacer matches to the marine vent virome suggest that viruses infecting hosts from diverse taxonomic groups are present in this vent environment. Comparative virome analyses show that CRISPR spacers from vent isolates and from thermophiles in general have a higher percentage of matches to the vent virome than to other marine or terrestrial hot spring viromes. However, a high percentage of hits to spacers from mesophilic hosts, combined with a moderately high modeled alpha diversity, suggest that the marine vent virome is comprised of viruses that have the potential to infect diverse taxonomic groups of multiple thermal regimes in both the bacterial and the archaeal domains.
Little is known about evolutionary drivers of microbial populations in the warm subseafloor of deep-sea hydrothermal vents. Here we reconstruct 73 metagenome-assembled genomes (MAGs) from two geochemically distinct vent fields in the Mid-Cayman Rise to investigate patterns of genomic variation within subseafloor populations. Low-abundance populations with high intra-population diversity coexist alongside high-abundance populations with low genomic diversity, with taxonomic differences in patterns of genomic variation between the mafic Piccard and ultramafic Von Damm vent fields. Populations from Piccard are significantly enriched in nonsynonymous mutations, suggesting stronger purifying selection in Von Damm relative to Piccard. Comparison of nine Sulfurovum MAGs reveals two high-coverage, low-diversity MAGs from Piccard enriched in unique genes related to the cellular membrane, suggesting these populations were subject to distinct evolutionary pressures that may correlate with genes related to nutrient uptake, biofilm formation, or viral invasion. These results are consistent with distinct evolutionary histories between geochemically different vent fields, with implications for understanding evolutionary processes in subseafloor microbial populations.
Microbial sulfur metabolism contributes to biogeochemical cycling on global scales. Sulfur metabolizing microbes are infected by phages that can encode auxiliary metabolic genes (AMGs) to alter sulfur metabolism within host cells but remain poorly characterized. Here we identified 191 phages derived from twelve environments that encoded 227 AMGs for oxidation of sulfur and thiosulfate (dsrA, dsrC/tusE, soxC, soxD and soxYZ). Evidence for retention of AMGs during niche-differentiation of diverse phage populations provided evidence that auxiliary metabolism imparts measurable fitness benefits to phages with ramifications for ecosystem biogeochemistry. Gene abundance and expression profiles of AMGs suggested significant contributions by phages to sulfur and thiosulfate oxidation in freshwater lakes and oceans, and a sensitive response to changing sulfur concentrations in hydrothermal environments. Overall, our study provides fundamental insights on the distribution, diversity, and ecology of phage auxiliary metabolism associated with sulfur and reinforces the necessity of incorporating viral contributions into biogeochemical configurations.
Many decades of experimental and theoretical research on the origin of life have yielded important discoveries regarding the chemical and physical conditions under which organic compounds can be synthesized and polymerized. However, such conditions often seem mutually exclusive, because they are rarely encountered in a single environmental setting. As such, no convincing models explain how living cells formed from abiotic constituents. Here, we propose a new approach that considers the origin of life within the global context of the Hadean Earth. We review previous ideas and synthesize them in four central hypotheses: (i) Multiple microenvironments contributed to the building blocks of life, and these niches were not necessarily inhabitable by the first organisms; (ii) Mineral catalysts were the backbone of prebiotic reaction networks that led to modern metabolism; (iii) Multiple local and global transport processes were essential for linking reactions occurring in separate locations; (iv) Global diversity and local selection of reactants and products provided mechanisms for the generation of most of the diverse building blocks necessary for life. We conclude that no single environmental setting can offer enough chemical and physical diversity for life to originate. Instead, any plausible model for the origin of life must acknowledge the geological complexity and diversity of the Hadean Earth. Future research may therefore benefit from identifying further linkages between organic precursors, minerals, and fluids in various environmental contexts.
Physical and chemical gradients are dominant factors in shaping hydrothermal vent microbial ecology, where archaeal and bacterial habitats encompass a range between hot, reduced hydrothermal fluid and cold, oxidized seawater. To determine the impact of these fluid gradients on microbial communities inhabiting these systems, we surveyed bacterial and archaeal community structure among and between hydrothermal plumes, diffuse flow fluids, and background seawater in several hydrothermal vent sites on the Juan de Fuca Ridge using 16S rRNA gene diversity screening (clone libraries and terminal restriction length polymorphisms) and quantitative polymerase chain reaction methods. Community structure was similar between hydrothermal plumes and background seawater, where a number of taxa usually associated with low-oxygen zones were observed, whereas high-temperature diffuse fluids exhibited a distinct phylogenetic profile. SUP05 and Arctic96BD-19 sulfur-oxidizing bacteria were prevalent in all three mixing regimes where they exhibited overlapping but not identical abundance patterns. Taken together, these results indicate conserved patterns of redox-driven niche partitioning between hydrothermal mixing regimes and microbial communities associated with sinking particles and oxygen-deficient waters. Moreover, the prevalence of SUP05 and Arctic96BD-19 in plume and diffuse flow fluids indicates a more cosmopolitan role for these groups in the ecology and biogeochemistry of the dark ocean.
28Environmental gradients generate countless ecological niches in deep-sea 29 hydrothermal vent systems, which foster diverse microbial communities. The majority of 30 distinct microbial lineages in these communities occur in very low abundance. However, 31 the ecological role and distribution of rare and abundant lineages, particularly in deep, 32 hot subsurface environments, remains unclear. Here, we use 16S rRNA tag sequencing to 33 describe biogeographic patterning and microbial community structure of both rare and 34 abundant archaea and bacteria in hydrothermal vent systems. We show that while rare 35 archaeal lineages and almost all bacterial lineages displayed geographically restricted 36 community structuring patterns, the abundant lineages of archaeal communities displayed 37 a much more cosmopolitan distribution.
The deep-sea hydrothermal vent habitat hosts a diverse community of archaea and bacteria that withstand extreme fluctuations in environmental conditions. Abundant viruses in these systems, a high proportion of which are lysogenic, must also withstand these environmental extremes. Here, we explore the evolutionary strategies of both microorganisms and viruses in hydrothermal systems through comparative analysis of a cellular and viral metagenome, collected by size fractionation of high temperature fluids from a diffuse flow hydrothermal vent. We detected a high enrichment of mobile elements and proviruses in the cellular fraction relative to microorganisms in other environments. We observed a relatively high abundance of genes related to energy metabolism as well as cofactors and vitamins in the viral fraction compared to the cellular fraction, which suggest encoding of auxiliary metabolic genes on viral genomes. Moreover, the observation of stronger purifying selection in the viral versus cellular gene pool suggests viral strategies that promote prolonged host integration. Our results demonstrate that there is great potential for hydrothermal vent viruses to integrate into hosts, facilitate horizontal gene transfer, and express or transfer genes that manipulate the hosts’ functional capabilities.
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