Autotrophic biofilms sustained by deeply sourced groundwater host diverse bacteria implicated in sulfur and hydrogen metabolism

Valentin-Alvarado, Luis E.; Fakra, Sirine C.; Probst, Alexander J.; Giska, Jonathan R.; Jaffe, Alexander L.; Oltrogge, Luke M.; West-Roberts, Jacob; Rowland, Joel; Manga, Michael; Savage, David F.; Greening, Chris; Baker, Brett J.; Banfield, Jillian F.

doi:10.1186/s40168-023-01704-w

Title: Autotrophic biofilms sustained by deeply sourced groundwater host diverse bacteria implicated in sulfur and hydrogen metabolism

Journal Article · 25 January 2024 · Microbiome

DOI: https://doi.org/10.1186/s40168-023-01704-w · OSTI ID:2282910

Valentin-Alvarado, Luis E.; Fakra, Sirine C.; Probst, Alexander J.; Giska, Jonathan R.; Jaffe, Alexander L.; Oltrogge, Luke M.; West-Roberts, Jacob; Rowland, Joel; Manga, Michael; Savage, David F.; Greening, Chris; Baker, Brett J.; Banfield, Jillian F.

Abstract Background Biofilms in sulfide-rich springs present intricate microbial communities that play pivotal roles in biogeochemical cycling. We studied chemoautotrophically based biofilms that host diverse CPR bacteria and grow in sulfide-rich springs to investigate microbial controls on biogeochemical cycling. Results Sulfide springs biofilms were investigated using bulk geochemical analysis, genome-resolved metagenomics, and scanning transmission X-ray microscopy (STXM) at room temperature and 87 K. Chemolithotrophic sulfur-oxidizing bacteria, including Thiothrix and Beggiatoa , dominate the biofilms, which also contain CPR Gracilibacteria, Absconditabacteria, Saccharibacteria, Peregrinibacteria, Berkelbacteria, Microgenomates, and Parcubacteria. STXM imaging revealed ultra-small cells near the surfaces of filamentous bacteria that may be CPR bacterial episymbionts. STXM and NEXAFS spectroscopy at carbon K and sulfur L _2,3 edges show that filamentous bacteria contain protein-encapsulated spherical elemental sulfur granules, indicating that they are sulfur oxidizers, likely Thiothrix . Berkelbacteria and Moranbacteria in the same biofilm sample are predicted to have a novel electron bifurcating group 3b [NiFe]-hydrogenase, putatively a sulfhydrogenase, potentially linked to sulfur metabolism via redox cofactors. This complex could potentially contribute to symbioses, for example, with sulfur-oxidizing bacteria such as Thiothrix that is based on cryptic sulfur cycling. One Doudnabacteria genome encodes adjacent sulfur dioxygenase and rhodanese genes that may convert thiosulfate to sulfite. We find similar conserved genomic architecture associated with CPR bacteria from other sulfur-rich subsurface ecosystems. Conclusions Our combined metagenomic, geochemical, spectromicroscopic, and structural bioinformatics analyses of biofilms growing in sulfide-rich springs revealed consortia that contain CPR bacteria and sulfur-oxidizing Proteobacteria, including Thiothrix , and bacteria from a new family within Beggiatoales. We infer roles for CPR bacteria in sulfur and hydrogen cycling.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: National Human Genome Research Institute; National Institutes of Health (NIH); National Science Foundation (NSF); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2282910

Journal Information:: Microbiome, Journal Name: Microbiome Journal Issue: 1 Vol. 12; ISSN 2049-2618

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds Finster, Kai Waldemar; Kjeldsen, Kasper Urup; Kube, Michael Standards in Genomic Sciences, Vol. 8, Issue 1 https://doi.org/10.4056/sigs.3777412	journal	April 2013
Gut bacteria are rarely shared by co-hospitalized premature infants, regardless of necrotizing enterocolitis development Raveh-Sadka, Tali; Thomas, Brian C.; Singh, Andrea eLife, Vol. 4 https://doi.org/10.7554/eLife.05477	journal	March 2015
MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies Kang, Dongwan D.; Li, Feng; Kirton, Edward PeerJ, Vol. 7 https://doi.org/10.7717/peerj.7359	journal	January 2019

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