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.
Summary
The structure and function of microbial communities inhabiting the subseafloor near hydrothermal systems are influenced by fluid geochemistry, geologic setting and fluid flux between vent ...sites, as well as biological interactions. Here, we used genome‐resolved metagenomics and metatranscriptomics to examine patterns of gene abundance and expression and assess potential niche differentiation in microbial communities in venting fluids from hydrothermal vent sites at the Mid‐Cayman Rise. We observed similar patterns in gene and transcript abundance between two geochemically distinct vent fields at the community level but found that each vent site harbours a distinct microbial community with differing transcript abundances for individual microbial populations. Through an analysis of metabolic pathways in 64 metagenome‐assembled genomes (MAGs), we show that MAG transcript abundance can be tied to differences in metabolic pathways and to potential metabolic interactions between microbial populations, allowing for niche‐partitioning and divergence in both population distribution and activity. Our results illustrate that most microbial populations have a restricted distribution within the seafloor, and that the activity of those microbial populations is tied to both genome content and abiotic factors.
Phosphorus plays a crucial role in controlling biological productivity, but geological estimates of phosphate concentrations in the Precambrian ocean, during life's origin and early evolution, vary ...over several orders of magnitude. While reduced phosphorus species may have served as alternative substrates to phosphate, their bioavailability on the early Earth remains unknown. Here, we reconstruct the phylogenomic record of life on Earth and find that phosphate transporting genes (pnas) evolved in the Paleoarchean (ca. 3.6-3.2 Ga) and are consistent with phosphate concentrations above modern levels ( > 3 µM). The first gene optimized for low phosphate levels (pstS; <1 µM) appeared around the same time or in the Mesoarchean depending on the reconstruction method. Most enzymatic pathways for metabolising reduced phosphorus emerged and expanded across the tree of life later. This includes phosphonate-catabolising CP-lyases, phosphite-oxidising pathways and hypophosphite-oxidising pathways. CP-lyases are particularly abundant in dissolved phosphate concentrations below 0.1 µM. Our results thus indicate at least local regions of declining phosphate levels through the Archean, possibly linked to phosphate-scavenging Fe(III), which may have limited productivity. However, reduced phosphorus species did not become widely used until after the Paleoproterozoic Great Oxidation Event (2.3 Ga), possibly linked to expansion of the biosphere at that time.
Environmental gradients generate countless ecological niches in deep-sea hydrothermal vent systems, which foster diverse microbial communities. The majority of distinct microbial lineages in these ...communities occur in very low abundance. However, the ecological role and distribution of rare and abundant lineages, particularly in deep, hot subsurface environments, remain unclear. Here, we use 16S rRNA tag sequencing to describe biogeographic patterning and microbial community structure of both rare and abundant archaea and bacteria in hydrothermal vent systems. We show that while rare archaeal lineages and almost all bacterial lineages displayed geographically restricted community structuring patterns, the abundant lineages of archaeal communities displayed a much more cosmopolitan distribution. Finally, analysis of one high-volume, high-temperature fluid sample representative of the deep hot biosphere described a unique microbial community that differed from microbial populations in diffuse flow fluid or sulfide samples, yet the rare thermophilic archaeal groups showed similarities to those that occur in sulfides. These results suggest that while most archaeal and bacterial lineages in vents are rare and display a highly regional distribution, a small percentage of lineages, particularly within the archaeal domain, are successful at widespread dispersal and colonization.
Rare and abundant strains of archaea and bacteria display different biogeographic patterns in hydrothermal vent systems.
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.
The deep marine subsurface constitutes a massive biosphere that hosts a multitude of archaea, bacteria, and viruses across a diversity of habitats. These microbes play key roles in mediating global ...biogeochemical cycles, and the marine subsurface is thought to have been among the earliest habitats for life on Earth. Yet we have a poor understanding of what forces govern the evolution of subsurface microbes over time. Here, I outline why evolutionary trajectories in the subsurface may be different than those of microbes living on the surface of the planet and describe how we can take advantage of technological advancements to study the evolutionary dynamics of subsurface microbes and their viruses. The sequencing revolution, in tandem with marine infrastructure advancements, promises that we will soon gain a much deeper understanding of how the vast majority of the microbial biosphere changes, adapts, and evolves over time.
The microbial communities of lake sediments have the potential to serve as valuable bioindicators and integrators of watershed land-use and water quality; however, the relative sensitivity of these ...communities to physio-chemical and geographical parameters must be demonstrated at taxonomic resolutions that are feasible by current sequencing and bioinformatic approaches. The geologically diverse and lake-rich state of Minnesota (USA) is uniquely situated to address this potential because of its variability in ecological region, lake type, and watershed land-use. In this study, we selected twenty lakes with varying physio-chemical properties across four ecological regions of Minnesota. Our objectives were to (i) evaluate the diversity and composition of the bacterial community at the sediment-water interface and (ii) determine how lake location and watershed land-use impact aqueous chemistry and influence bacterial community structure. Our 16S rRNA amplicon data from lake sediment cores, at two depth intervals, data indicate that sediment communities are more likely to cluster by ecological region rather than any individual lake properties (e.g., trophic status, total phosphorous concentration, lake depth). However, composition is tied to a given lake, wherein samples from the same core were more alike than samples collected at similar depths across lakes. Our results illustrate the diversity within lake sediment microbial communities and provide insight into relationships between taxonomy, physicochemical, and geographic properties of north temperate lakes.
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.
Abstract
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.
Hydrogenotrophic methanogens are ubiquitous chemoautotrophic archaea inhabiting globally distributed deep-sea hydrothermal vent ecosystems and associated subseafloor niches within the rocky ...subseafloor, yet little is known about how they adapt and diversify in these habitats. To determine genomic variation and selection pressure within methanogenic populations at vents, we examined five
Methanothermococcus
single cell amplified genomes (SAGs) in conjunction with 15 metagenomes and 10 metatranscriptomes from venting fluids at two geochemically distinct hydrothermal vent fields on the Mid-Cayman Rise in the Caribbean Sea. We observed that some
Methanothermococcus
lineages and their transcripts were more abundant than others in individual vent sites, indicating differential fitness among lineages. The relative abundances of lineages represented by SAGs in each of the samples matched phylogenetic relationships based on single-copy universal genes, and genes related to nitrogen fixation and the CRISPR/Cas immune system were among those differentiating the clades. Lineages possessing these genes were less abundant than those missing that genomic region. Overall, patterns in nucleotide variation indicated that the population dynamics of
Methanothermococcus
were not governed by clonal expansions or selective sweeps, at least in the habitats and sampling times included in this study. Together, our results show that although specific lineages of
Methanothermococcus
co-exist in these habitats, some outcompete others, and possession of accessory metabolic functions does not necessarily provide a fitness advantage in these habitats in all conditions. This work highlights the power of combining single-cell, metagenomic, and metatranscriptomic datasets to determine how evolution shapes microbial abundance and diversity in hydrothermal vent ecosystems.
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