Biology subjects

Banfield, J. F.

Publications and source records attributed to Banfield, J. F..

At least 55 records · Page 3Linked to original sources

bioRxiv2021

Borgs are giant extrachromosomal elements with the potential to augment methane oxidation

Anaerobic methane oxidation exerts a key control on greenhouse gas emissions 1, yet factors that modulate the activity of microorganisms performing this function remain little explored. In studying groundwater, sediments, and wetland soil where methane production and oxidation occur, we discovered extraordinarily large, diverse DNA sequences that primarily encode hypothetical proteins. Four curated, complete genomes are linear, up to ~1 Mbp in length and share genome organization, including replicore structure, long inverted terminal repeats, and genome-wide unique perfect tandem direct repeats that are intergenic or generate amino acid repeats. We infer that these are a new type of archaeal extrachromosomal element with a distinct evolutionary origin. Gene sequence similarity, phylogeny, and local divergence of sequence composition indicate that many of their genes were assimilated from methane-oxidizing Methanoperedens archaea. We refer to these elements as "Borgs". We identified at least 19 different Borg types coexisting with Methanoperedens in four distinct ecosystems. Borg genes expand redox and respiratory capacity (e.g., clusters of multiheme cytochromes), ability to respond to changing environmental conditions, and likely augment Methanoperedens capacity for methane oxidation (e.g., methyl coenzyme M reductase). By this process, Borgs could play a previously unrecognized role in controlling greenhouse gas emissions.

microbiology↗

bioRxiv2021

Syntrophic H2 production enhances the performance of primarily acetate-supplemented reactors treating sulphate contaminated solutions

Biological sulfate reduction (BSR) represents a promising bioremediation strategy, yet the impact of metabolic interactions on performance has been largely unexplored. Here, genome-resolved metagenomics was used to characterise 17 microbial communities associated with reactors operated with defined sulfate-contaminated solutions. Pairs of reactors were supplemented with lactate or with acetate plus a small amount of fermentable substrate. At least thirty draft quality genomes, representing all the abundant bacteria, were recovered from each metagenome. All of the 22 SRB genomes encode genes for H2 consumption. And of the total 163 genomes recovered, 130 encode 321 NiFe and FeFe hydrogenases. The lactate-supplemented packed-bed bioreactor was particularly interesting as it resulted in stratified microbial communities that were distinct in their predominant metabolisms. Pathways for fermentation of lactate and hydrogen production were enriched towards the inlet whereas increased autotrophy and acetate-oxidizing SRB were evident towards the end of the flow path. We hypothesized that high sulfate removal towards the end of the flow path, despite acetate being an electron donor that typically sustains low SRB growth rates, was stimulated by H2 consumption. This hypothesis was supported by sustained performance of the predominantly acetate-supplemented stirred-tank reactor, which was dominated by diverse fermentative, hydrogen-evolving bacteria and low-abundance SRB capable of acetate and hydrogen consumption. We conclude that the performance of BSR reactors supplemented with inexpensive acetate can be improved by the addition of a low concentration of fermentable material due to stimulation of syntrophic relationships among hydrogen-producing non-SRB and dual hydrogen- and acetate-utilising SRB.

microbiology↗

bioRxiv2021

A widely distributed genus of soil Acidobacteria genomically enriched in biosynthetic gene clusters

Bacteria of the phylum Acidobacteria are one of the most abundant bacterial across soil ecosystems, yet they are represented by comparatively few sequenced genomes, leaving gaps in our understanding of their metabolic diversity. Recently, genomes of Acidobacteria species with unusually large repertoires of biosynthetic gene clusters (BGCs) were reconstructed from grassland soil metagenomes, but the degree to which these species are widespread is still unknown. To investigate this, we augmented a dataset of publicly available Acidobacteria genomes with 46 metagenome-assembled genomes recovered from permanently saturated organic-rich soils of a vernal (spring) pool ecosystem in Northern California. We recovered high quality genomes for three novel species from Candidatus Angelobacter (a proposed subdivision 1 Acidobacterial genus), a genus that is genomically enriched in genes for specialized metabolite biosynthesis. Acidobacteria were particularly abundant in the vernal pool sediments, and a Ca. Angelobacter species was the most abundant bacterial species detected in some samples. We identified numerous diverse biosynthetic gene clusters in these genomes, and also in additional genomes from other publicly available soil metagenomes for other related Ca. Angelobacter species. Metabolic analysis indicates that Ca. Angelobacter likely are aerobes that ferment organic carbon, with potential to contribute to carbon compound turnover in soils. Using metatranscriptomics, we identified in situ expression of specialized metabolic traits for two species from this genus. In conclusion, we expand genomic sampling of the uncultivated Ca. Angelobacter, and show that they represent common and sometimes highly abundant members of dry and saturated soil communities, with a high degree of capacity for synthesis of diverse specialized metabolites.

microbiology↗

bioRxiv2021

Soils and sediments host novel archaea with divergent monooxygenases implicated in ammonia oxidation

Copper membrane monooxygenases (CuMMOs) play critical roles in the global carbon and nitrogen cycles. Organisms harboring these enzymes perform the first, and rate limiting, step in aerobic oxidation of ammonia, methane, or other simple hydrocarbons. Within archaea, only organisms in the order Nitrososphaerales (Thaumarchaeota) encode CuMMOs, which function exclusively as ammonia monooxygenases. From grassland and hillslope soils and aquifer sediments, we identified 20 genomes from distinct archaeal species encoding divergent CuMMO sequences. These archaea are phylogenetically clustered in a previously unnamed Thermoplasmatota order, herein named the Ca. Angelarcheales. The CuMMO proteins in Ca. Angelarcheales are more similar in structure to those in ammonia-oxidizing archaea than those of bacteria, and they contain all functional residues required for activity. Similarly to the Nitrososphaerales, Ca. Angelarcheales genomes are significantly enriched in blue copper proteins (BCPs) relative to sibling lineages, including plastocyanin-like electron carriers and divergent nitrite reductase-like (nirK) 2-domain cupredoxin proteins co-located with electron transport machinery. Angelarcheales do not have identifiable genes for methanol oxidation or carbon fixation, encode significant capacity for peptide/amino acid uptake and degradation, and share numerous electron transport mechanisms with the Nitrososphaerales. In the studied soils and sediments Ca. Angelarcheales were at least as abundant as ammonia-oxidizing Nitrososphaerales. Thus, we predict that Angelarcheales live a mixotrophic lifestyle based on oxidation of ammonia liberated from peptide and amino acid degradation. This work expands the known diversity of Thermoplasmatota and of CuMMO enzymes in archaea and suggests that these organisms are important and previously unaccounted for contributors to nitrogen cycling.

microbiology↗

bioRxiv2021

Patterns of gene content and co-occurrence constrain the evolutionary path toward animal association in CPR bacteria

Candidate Phyla Radiation (CPR) bacteria are small, likely episymbiotic organisms found across Earths ecosystems. Despite their prevalence, the distribution of CPR lineages across habitats and the genomic signatures of transitions amongst these habitats remain unclear. Here, we expand the genome inventory for Absconditabacteria (SR1), Gracilibacteria, and Saccharibacteria (TM7), CPR bacteria known to occur in both animal-associated and environmental microbiomes, and investigate variation in gene content with habitat of origin. By overlaying phylogeny with habitat information, we show that bacteria from these three lineages have undergone multiple transitions from environmental habitats into animal microbiomes. Based on co-occurrence analyses of hundreds of metagenomes, we extend the prior suggestion that certain Saccharibacteria have broad bacterial host ranges and constrain possible host relationships for Absconditabacteria and Gracilibacteria. Full-proteome analyses show that animal-associated Saccharibacteria have smaller gene repertoires than their environmental counterparts and are enriched in numerous protein families, including those likely functioning in amino acid metabolism, phage defense, and detoxification of peroxide. In contrast, some freshwater Saccharibacteria encode a putative rhodopsin. For protein families exhibiting the clearest patterns of differential habitat distribution, we compared protein and species phylogenies to estimate the incidence of lateral gene transfer and genomic loss occurring over the species tree. These analyses suggest that habitat transitions were likely not accompanied by large transfer or loss events, but rather were associated with continuous proteome remodeling. Thus, we speculate that CPR habitat transitions were driven largely by availability of suitable host taxa, and were reinforced by acquisition and loss of some capacities. IMPORTANCEStudying the genetic differences between related microorganisms from different environment types can indicate factors associated with their movement among habitats. This is particularly interesting for bacteria from the Candidate Phyla Radiation because their minimal metabolic capabilities require symbiotic associations with microbial hosts. We found that shifts of Absconditabacteria, Gracilibacteria, and Saccharibacteria between environmental ecosystems and mammalian mouths/guts probably did not involve major episodes of gene gain and loss; rather, gradual genomic change likely followed habitat migration. The results inform our understanding of how little-known microorganisms establish in the human microbiota where they may ultimately impact health.

microbiology↗

bioRxiv2021

Infant gut strain persistence is associated with maternal origin, phylogeny, and functional potential including surface adhesion and iron acquisition

Gut microbiome succession impacts infant development. However, it remains unclear what factors promote persistence of initial bacterial colonists in the developing gut. Here, we performed strain-resolved metagenomic analyses to compare gut colonization of preterm and full-term infants throughout the first year of life and evaluated links between strain persistence and strain origin as well as genetic potential. Analysis of 206 fecal metagenomes collected from full-term and preterm infants and their mothers revealed that infants initially distinct microbial communities converged by age one. Approximately 11% of early colonists, primarily Bacteroides and Bifidobacterium, persisted during the first year of life, and these were more prevalent in full-term compared to preterm infants. Gut-associated strains from mothers were significantly more likely to persist in the infant gut than other strains. Enrichment in genes for surface adhesion, iron acquisition and carbohydrate degradation may explain persistence of some strains through the first year of life.

microbiology↗

bioRxiv2021

Wide distribution of alternatively coded Lak megaphages in animal microbiomes

Lak phages with alternatively coded ~540 kbp genomes were recently reported to replicate in Prevotella in the gut microbiomes of humans that consume a non-western diet, baboons and some pigs. Here, we investigate the diversity and broader distribution of Lak phages in human and animal microbiomes using diagnostic PCR and genome-resolved metagenomics. Lak phages were detected in 13 different animal types and are particularly prevalent in pigs, with significant enrichment in the hindgut compared to foregut. We reconstructed 34 new Lak genomes, including six curated complete genomes, all of which are alternatively coded. The most deeply branched Lak is from a horse faecal sample and is the largest phage genome from an animal microbiome (~660 kbp). From the Lak genomes, we identified families of hypothetical proteins associated with specific animal types. Overall, we substantially expanded Lak phage diversity and demonstrate their occurrence in a variety of human and animal microbiomes.

microbiology↗

bioRxiv2020

Structural coordination between active sites of a Cas6-reverse transcriptase-Cas1--Cas2 CRISPR integrase complex

CRISPR-Cas systems provide adaptive immunity in bacteria and archaea by targeting foreign DNA for destruction using CRISPR RNA-guided enzymes. CRISPR immunity begins with integration of foreign sequences into the host CRISPR genomic locus, followed by transcription and maturation of CRISPR RNAs. In a few CRISPR systems, the Cas1 integrase and a Cas6 nuclease are fused to a reverse transcriptase that enables viral sequence acquisition from both DNA and RNA sources. To determine how these components work together, we determined a 3.7 [A] resolution cryo-EM structure of a Cas6-RT-Cas1 protein complexed with Cas2, a subunit of the CRISPR integrase. The structure and accompanying mutagenesis experiments provide evidence of bidirectional crosstalk between the Cas1 and RT active sites and unidirectional crosstalk from Cas6 to the Cas1 and RT active sites. Together, these findings suggest regulated structural rearrangements that may coordinate the complexs different enzymatic activities.

biochemistry↗

bioRxiv2020

Stable isotope informed genome-resolved metagenomics uncovers potential trophic interactions in rhizosphere soil

The functioning, health, and productivity of soil is intimately tied to a complex network of interactions, particularly in plant root-associated rhizosphere soil. We conducted a stable isotope-informed, genome-resolved metagenomic study to trace carbon from Avena fatua grown in a 13CO2 atmosphere into soil. We collected paired rhizosphere and non-rhizosphere soil at six and nine weeks of plant growth and extracted DNA that was then separated by density using gradient centrifugation. Thirty-two fractions from each sample were grouped by density, sequenced, assembled, and binned to generate 55 unique microbial genomes that were >70% complete. The complete 18S rRNA sequences of several micro-eukaryotic bacterivores and fungi were enriched in 13C. We generated several circularized bacteriophage (phage) genomes, some of which were the most labelled entities in the rhizosphere. CRISPR locus targeting connected one of these phage to a Burkholderiales host predicted to be a plant pathogen. Another highly labeled phage is predicted to replicate in a Catenulispora sp., a possible plant growth-promoting bacterium. We searched the genomes for traits known to be used in interactions involving bacteria, micro-eukaryotes and plant roots and found that heavily isotopically-labeled bacteria have the ability to modulate plant signaling hormones, possess numerous plant pathogenicity factors, and produce toxins targeting micro-eukaryotes. Overall, 13C stable isotope-informed genome-resolved metagenomics revealed that very active bacteria often have the potential for strong interactions with plants and directly established that phage can be important agents of turnover of plant-derived carbon in soil.

microbiology↗

bioRxiv2020

Early acquisition of conserved, lineage-specific proteins currently lacking functional predictions were central to the rise and diversification of archaea

Recent genomic analyses of Archaea have profoundly reshaped our understanding of their distribution, functionalities and roles in eukaryotic evolution. Within the domain, major supergroups are Euryarchaeota, which includes many methanogens, the TACK, which includes Thaumarchaeaota that impact ammonia oxidation in soils and the ocean, the Asgard, which includes lineages inferred to be ancestral to eukaryotes, and the DPANN, a group of mostly symbiotic small-celled archaea. Here, we investigated the extent to which clustering based on protein family content recapitulates archaeal phylogeny and identified the proteins that distinguish the major subdivisions. We also defined 10,866 archaeal protein families that will serve as a community resource. Clustering based on these families broadly recovers the archaeal phylogenetic tree. Interestingly, all major groups are distinguished primarily by the presence of families of conserved hypothetical proteins that are either novel or so highly diverged that their functions are obscured. Given that these hypothetical proteins are near ubiquitous within phyla, we conclude that they were important in the origin of most of the major archaeal lineages.

microbiology↗

bioRxiv2020

Targeted Genome Editing of Bacteria Within Microbial Communities

Knowledge of microbial gene functions comes from manipulating the DNA of individual species in isolation from their natural communities. While this approach to microbial genetics has been foundational, its requirement for culturable microorganisms has left the majority of microbes and their interactions genetically unexplored. Here we describe a generalizable methodology for editing the genomes of specific organisms within a complex microbial community. First, we identified genetically tractable bacteria within a community using a new approach, Environmental Transformation Sequencing (ET-Seq), in which non-targeted transposon integrations were mapped and quantified following community delivery. ET-Seq was repeated with multiple delivery strategies for both a nine-member synthetic bacterial community and a ~200-member microbial bioremediation community. We achieved insertions in 10 species not previously isolated and identified natural competence for foreign DNA integration that depends on the presence of the community. Second, we developed and used DNA-editing All-in-one RNA-guided CRISPR-Cas Transposase (DART) systems for targeted DNA insertion into organisms identified as tractable by ET-Seq, enabling organism- and locus-specific genetic manipulation within the community context. These results demonstrate a strategy for targeted genome editing of specific organisms within microbial communities, establishing a new paradigm for microbial manipulation relevant to research and applications in human, environmental, and industrial microbiomes.

microbiology↗

bioRxiv2020

Unexpected diversity of CPR bacteria and nanoarchaea in the rare biosphere of rhizosphere-associated grassland soil

Candidate Phyla Radiation (CPR) bacteria and nanoarchaea populate most ecosystems, but are rarely detected in soil. We concentrated particles less than 0.2 m from grassland soil, enabling targeted metagenomic analysis of these organisms, which are almost totally unexplored in soil. We recovered a diversity of CPR bacteria and some nanoarchaea sequences, but no sequences from other cellular organisms. The sampled sequences include Doudnabacteria (SM2F11) and Pacearchaeota, organisms not previously reported in soil, as well as Saccharibacteria, Parcubacteria and Microgenomates. CPR and DPANN (an acronym of the names of the first included archaea phyla) enrichments of 100-1000-fold were achieved compared to bulk soil, in which we estimate these organisms comprise about 1 to 100 cells per gram of soil. Like most CPR and DPANN sequenced to date, we predict these microorganisms live symbiotic, anaerobic lifestyles. However, Saccharibacteria, Parcubacteria, and Doudnabacteria genomes sampled here also encode ubiquinol oxidase operons that may have been acquired from other bacteria, likely during adaptation to aerobic soil environments. We posit that although present at low abundance, CPR bacteria and DPANN archaea could impact overall soil microbial community function by modulating host organism abundances and activity.

microbiology↗

bioRxiv2020

Transporter genes in biosynthetic gene clusters predict metabolite characteristics and siderophore activity

Biosynthetic gene clusters (BGCs) are operonic sets of microbial genes that synthesize specialized metabolites with diverse functions, including siderophores and antibiotics, which often require export to the extracellular environment. For this reason, genes for transport across cellular membranes are essential for the production of specialized metabolites, and are often genomically co-localized with BGCs. Here we conducted a comprehensive computational analysis of transporters associated with characterized BGCs. In addition to known exporters, in BGCs we found many importer-specific transmembrane domains that co-occur with substrate binding proteins possibly for uptake of siderophores or metabolic precursors. Machine learning models using transporter gene frequencies were predictive of known siderophore activity, molecular weights, and a measure of lipophilicity (log P) for corresponding BGC-synthesized metabolites. Transporter genes associated with BGCs were often equally or more predictive of metabolite features than biosynthetic genes. Given the importance of siderophores as pathogenicity factors, we used transporters specific for siderophore BGCs to identify both known and uncharacterized siderophore-like BGCs in genomes from metagenomes from the infant and adult gut microbiome. We find that 23% of microbial genomes from the infant gut have siderophore-like BGCs, but only 3% of those assembled from adult gut microbiomes do. While siderophore-like BGCs from the infant gut are predominantly associated with Enterobactericaee and Staphylococcus, siderophore-like BGCs can be identified from taxa in the adult gut microbiome that have rarely been recognized for siderophore production. Taken together, these results show that consideration of BGC-associated transporter genes can inform predictions of specialized metabolite structure and function.

bioinformatics↗

bioRxiv2020

Meanders as a scaling motif for understanding of floodplain soil microbiome and biogeochemical potential at the watershed scale

Biogeochemical exports of C, N, S and H2 from watersheds are modulated by the activity of microorganisms that function over micron scales. This disparity of scales presents a substantial challenge for development of predictive models describing watershed function. Here, we tested the hypothesis that meander-bound regions exhibit patterns of microbial metabolic potential that are broadly predictive of biogeochemical processes in floodplain soils along a river corridor. We intensively sampled floodplain soils located in the upper, middle, and lower reaches of the East River in Colorado and reconstructed 248 draft quality genomes representative at a sub-species level. Approximately one third of the representative genomes were detected across all three locations with similar levels of abundance, and despite the very high microbial diversity and complexity of the soils, ~15% of species were detected in two consecutive years. A core floodplain microbiome was enriched in bacterial capacities for aerobic respiration, aerobic CO oxidation, and thiosulfate oxidation with the formation of elemental sulfur. We did not detect systematic patterns of gene abundance based on sampling position relative to the river. However, at the watershed scale meander-bound floodplains appear to serve as scaling motifs that predict aggregate capacities for biogeochemical transformations in floodplain soils. Given this, we conducted a transcriptomic analysis of the middle site. Overall, the most highly transcribed genes were amoCAB and nxrAB (for nitrification) followed by genes involved in methanol and formate oxidation, and nitrogen and CO2 fixation. Low soil organic carbon correlated with high activity of genes involved in methanol, formate, sulfide, hydrogen, and ammonia oxidation, nitrite oxidoreduction, and nitrate and nitrite reduction. Thus, widely represented genetic capacities did not predict in situ activity at one time point, but rather they define a reservoir of biogeochemical potential available as conditions change.

microbiology↗

bioRxiv2020

Huge and variable diversity of episymbiotic CPR bacteria and DPANN archaea in groundwater ecosystems

Candidate Phyla Radiation (CPR) bacteria and DPANN archaea are uncultivated, small-celled symbionts often detected in groundwater. However, variations in CPR/DPANN organism abundance, distribution, taxonomic diversity, and degree/nature of host association with groundwater chemistry remain understudied. Here, we performed genome-resolved metagenomic characterization of one agriculturally-impacted and seven pristine groundwater microbial communities in California, recovering 746 dereplicated CPR and DPANN genomes. Our finding of up to 31% CPR bacteria and 4% DPANN archaea in the pristine sites, which serve as local sources of drinking water, may hold health relevance, given growing awareness of the presence of CPR/DPANN organisms in human microbiomes and their association with disease. There is little species-level genome overlap across groundwater sites, indicating that CPR and DPANN communities are highly differentiated according to host populations and physicochemical conditions. Cryo-TEM imaging and genomic analyses indicate that CPR growth may be stimulated by attachment to the surface of host cells, and identified CPR and DPANN lineages with particularly prevalent and/or resilient host cell attachment. These results establish the huge but site-specific diversity of CPR bacteria and DPANN archaea coexisting with diverse hosts in groundwater aquifers, and raise important questions about potential impacts on human health.

microbiology↗

bioRxiv2020

Thiocyanate and organic carbon inputs drive convergent selection for specific autotrophic Afipia and Thiobacillus strains within complex microbiomes

Thiocyanate (SCN-) contamination threatens aquatic ecosystems and pollutes vital fresh water supplies. SCN- degrading microbial consortia are commercially deployed for remediation, but the impact of organic amendments on selection within SCN- degrading microbial communities has not been investigated. Here, we tested whether specific strains capable of degrading SCN- could be reproducibly selected for based on SCN- loading and the presence or absence of added organic carbon. Complex microbial communities derived from those used to treat SCN- contaminated water were exposed to systematically increased input SCN concentrations in molasses-amended and -unamended reactors and in reactors switched to unamended conditions after establishing the active SCN- degrading consortium. Five experiments were conducted over 790 days and genome-resolved metagenomics was used to resolve community composition at the strain level. A single Thiobacillus strain proliferated in all reactors at high loadings. Despite the presence of many Rhizobiales strains, a single Afipia variant dominated the molasses-free reactor at moderately high loadings. This strain is predicted to breakdown SCN- using a novel thiocyanate dehydrogenase, oxidize resulting reduced sulfur, degrade product cyanate (OCN-) to ammonia and CO2 via cyanase, and fix CO2 via the Calvin-Benson-Bassham cycle. Removal of molasses from input feed solutions reproducibly led to dominance of this strain. Neither this Afipia strain nor the thiobacilli have the capacity to produce cobalamin, a function detected in low abundance community members. Although sustained by autotrophy, reactors without molasses did not stably degrade SCN- at high loading rates, perhaps due to loss of biofilm-associated niche diversity. Overall, convergence in environmental conditions led to convergence in the strain composition, although reactor history also impacted the trajectory of community compositional change.

microbiology↗

bioRxiv2020

Genetic and behavioral adaptation of Candida parapsilosis to the microbiome of hospitalized infants revealed by in situ genomics, transcriptomics and proteomics

Candida parapsilosis is a common cause of invasive candidiasis, especially in newborn infants, and infections have been increasing over the past two decades. C. parapsilosis has been primarily studied in pure culture, leaving gaps in understanding of its function in microbiome context. Here, we reconstructed five unique C. parapsilosis genomes from premature infant fecal samples and analyzed their genome structure, population diversity and in situ activity relative to reference strains in pure culture. All five genomes contain hotspots of single nucleotide variants, some of which are shared by strains from multiple hospitals. A subset of environmental and hospital-derived genomes share variants within these hotspots suggesting derivation of that region from a common ancestor. Four of the newly reconstructed C. parapsilosis genomes have four to sixteen copies of the gene RTA3, which encodes a lipid translocase and is implicated in antifungal resistance, potentially indicating adaptation to hospital antifungal use. Time course metatranscriptomics and metaproteomics on fecal samples from a premature infant with a C. parapsilosis blood infection revealed highly variable in situ expression patterns that are distinct from those of similar strains in pure cultures. For example, biofilm formation genes were relatively less expressed in situ, whereas genes linked to oxygen utilization were more highly expressed, indicative of growth in a relatively aerobic environment. In gut microbiome samples, C. parapsilosis coexisted with Enterococcus faecalis that shifted in relative abundance over time, accompanied by changes in bacterial and fungal gene expression and proteome composition. The results reveal potentially medically relevant differences in Candida function in gut vs. laboratory environments, and constrain evolutionary processes that could contribute to hospital strain persistence and transfer into premature infant microbiomes.

microbiology↗

bioRxiv2020

Genome-resolved metagenomics and detailed geochemical speciation analyses yield new insights into microbial mercury cycling in geothermal springs

Geothermal systems emit substantial amounts of aqueous, gaseous and methylated mercury, but little is known about microbial influences on mercury speciation. Here we report results from genome-resolved metagenomics and mercury speciation analysis of acid warm springs in the Ngawha Geothermal Field (<55 {degrees}C, pH < 4.5), Northland Region, Aotearoa (New Zealand). Our aim was to identify the microorganisms genetically equipped for mercury methylation, demethylation, or Hg(II) reduction to volatile Hg(0) in these springs. Dissolved total and methylated mercury concentrations in two adjacent springs with different mercury speciation ranked among the highest reported from natural sources (250-16000 ng L-1 and 0.5-13.9 ng L-1, respectively). Total solid mercury concentrations in spring sediments ranged from 1273 to 7000 {micro}g g-1. In the context of such ultra-high mercury levels, the geothermal microbiome was unexpectedly diverse, and dominated by acidophilic and mesophilic sulfur- and iron-cycling bacteria, mercury- and arsenic-resistant bacteria, and thermophilic and acidophilic archaea. Integrating microbiome structure and metagenomic potential with geochemical constraints, we constructed a conceptual model for biogeochemical mercury cycling in geothermal springs. The model includes abiotic and biotic controls on mercury speciation, and illustrates how geothermal mercury cycling may couple to microbial community dynamics and sulfur and iron biogeochemistry. IMPORTANCELittle is currently known about biogeochemical mercury cycling in geothermal systems. This manuscript presents an important new conceptual model, supported by genome-resolved metagenomic analysis and detailed geochemical measurements. This work provides a framework for studying natural geothermal mercury emissions globally. Specifically, our findings have implications for mercury speciation in wastewaters from geothermal power plants and the potential environmental impacts of microbially and abiotically formed mercury species, particularly where mobilized in spring waters that mix with surface- or ground-waters. Furthermore, in the context of thermophilic origins for microbial mercury volatilisation, this report yields new insights into how such processes may have evolved alongside microbial mercury methylation/demethylation, and the environmental constraints imposed by the geochemistry and mineralogy of geothermal systems.

microbiology↗