Meta-omics reveals role of photosynthesis in microbially induced carbonate precipitation at a CO2-rich geyser

Violette, Marlene J.; Hyland, Ethan; Burgener, Landon; Ghosh, Adit; Montoya, Brina M.; Kleiner, Manuel

doi:10.1093/ismeco/ycae139

Title: Meta-omics reveals role of photosynthesis in microbially induced carbonate precipitation at a CO2-rich geyser

Journal Article · 10 December 2024 · ISME Communications

DOI: https://doi.org/10.1093/ismeco/ycae139 · OSTI ID:2506788

Violette, Marlene J.; Hyland, Ethan; Burgener, Landon; Ghosh, Adit; Montoya, Brina M.; Kleiner, Manuel

Abstract Microbially induced carbonate precipitation (MICP) is a natural process with potential biotechnological applications to address both carbon sequestration and sustainable construction needs. However, our understanding of the microbial processes involved in MICP is limited to a few well-researched pathways such as ureolytic hydrolysis. To expand our knowledge of MICP, we conducted an omics-based study on sedimentary communities from travertine around the CO2-driven Crystal Geyser near Green River, Utah. Using metagenomics and metaproteomics, we identified the community members and potential metabolic pathways involved in MICP. We found variations in microbial community composition between the two sites we sampled, but Rhodobacterales were consistently the most abundant order, including both chemoheterotrophs and anoxygenic phototrophs. We also identified several highly abundant genera of Cyanobacteriales. The dominance of these community members across both sites and the abundant presence of photosynthesis-related proteins suggest that photosynthesis could play a role in MICP at Crystal Geyser. We also found abundant bacterial proteins involved in phosphorous starvation response at both sites suggesting that P-limitation shapes both composition and function of the microbial community driving MICP.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0022996

OSTI ID:: 2506788

Journal Information:: ISME Communications, Journal Name: ISME Communications Journal Issue: 1 Vol. 4; ISSN 2730-6151

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (64)

Multidomain ribosomal protein trees and the planctobacterial origin of neomura (eukaryotes, archaebacteria) Cavalier-Smith, Thomas; Chao, Ema E-Yung Protoplasma, Vol. 257, Issue 3 https://doi.org/10.1007/s00709-019-01442-7	journal	January 2020
Nitrogen Metabolism Genes from Temperate Marine Sediments Reyes, Carolina; Schneider, Dominik; Lipka, Marko Marine Biotechnology, Vol. 19, Issue 2 https://doi.org/10.1007/s10126-017-9741-0	journal	March 2017
Kinetic enrichment of stable isotopes in cryogenic calcites Clark, Ian D.; Lauriol, Bernard Chemical Geology, Vol. 102, Issue 1-4 https://doi.org/10.1016/0009-2541(92)90157-Z	journal	December 1992
13C and 18O isotopic disequilibrium in biological carbonates: I. Patterns McConnaughey, Ted Geochimica et Cosmochimica Acta, Vol. 53, Issue 1 https://doi.org/10.1016/0016-7037(89)90282-2	journal	January 1989
The composition of the continental crust Hans Wedepohl, K. Geochimica et Cosmochimica Acta, Vol. 59, Issue 7 https://doi.org/10.1016/0016-7037(95)00038-2	journal	April 1995
Active transport of maltose in Escherichia coli K12. Role of the periplasmic maltose-binding protein and evidence for a substrate recognition site in the cytoplasmic membrane. Shuman, H. A. Journal of Biological Chemistry, Vol. 257, Issue 10 https://doi.org/10.1016/S0021-9258(19)83799-7	journal	May 1982
Bioremediation of metal-contaminated soils by microbially-induced carbonate precipitation and its effects on ecotoxicity and long-term stability Liu, Peng; Zhang, Yu; Tang, Qiang Biochemical Engineering Journal, Vol. 166 https://doi.org/10.1016/j.bej.2020.107856	journal	February 2021
Photosynthetic isotope biosignatures in laminated micro-stromatolitic and non-laminated nodules associated with modern, freshwater microbialites in Pavilion Lake, B.C. Brady, A. L.; Slater, G. F.; Omelon, C. R. Chemical Geology, Vol. 274, Issue 1-2 https://doi.org/10.1016/j.chemgeo.2010.03.016	journal	June 2010
Calcium carbonate precipitation by anoxygenic phototrophic bacteria Bundeleva, Irina A.; Shirokova, Liudmila S.; Bénézeth, Pascale Chemical Geology, Vol. 291 https://doi.org/10.1016/j.chemgeo.2011.10.003	journal	January 2012
Bacillus subtilis bacteria used in fiber reinforced concrete and their effects on concrete penetrability Karimi, Nasrin; Mostofinejad, Davood Construction and Building Materials, Vol. 230 https://doi.org/10.1016/j.conbuildmat.2019.117051	journal	January 2020
Potential soil reinforcement by biological denitrification van Paassen, Leon A.; Daza, Claudia M.; Staal, Marc Ecological Engineering, Vol. 36, Issue 2 https://doi.org/10.1016/j.ecoleng.2009.03.026	journal	February 2010
Periodic changes in effluent chemistry at cold-water geyser: Crystal geyser in Utah Han, Weon Shik; Watson, Z. T.; Kampman, Niko Journal of Hydrology, Vol. 550 https://doi.org/10.1016/j.jhydrol.2017.04.030	journal	July 2017
Global regulation by the seven-component Pi signaling system Hsieh, Yi-Ju; Wanner, Barry L. Current Opinion in Microbiology, Vol. 13, Issue 2 https://doi.org/10.1016/j.mib.2010.01.014	journal	April 2010
Microbial mats as bioreactors: populations, processes, and products Visscher, Pieter T.; Stolz, John F. Palaeogeography, Palaeoclimatology, Palaeoecology, Vol. 219, Issue 1-2 https://doi.org/10.1016/j.palaeo.2004.10.016	journal	April 2005
Optimized Extraction Method To Remove Humic Acid Interferences from Soil Samples Prior to Microbial Proteome Measurements Qian, Chen; Hettich, Robert L. Journal of Proteome Research, Vol. 16, Issue 7 https://doi.org/10.1021/acs.jproteome.7b00103	journal	June 2017
Oceanic Methane Biogeochemistry Reeburgh, William S. Chemical Reviews, Vol. 107, Issue 2 https://doi.org/10.1021/cr050362v	journal	February 2007
The Solubility of Silica. Lenher, Victor; Merrill, Henry Baldwin Journal of the American Chemical Society, Vol. 39, Issue 12 https://doi.org/10.1021/ja02257a013	journal	December 1917
Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea Bowers, Robert M.; Kyrpides, Nikos C.; Stepanauskas, Ramunas Nature Biotechnology, Vol. 35, Issue 8 https://doi.org/10.1038/nbt.3893	journal	August 2017
Universal sample preparation method for proteome analysis Wiśniewski, Jacek R.; Zougman, Alexandre; Nagaraj, Nagarjuna Nature Methods, Vol. 6, Issue 5 https://doi.org/10.1038/nmeth.1322	journal	April 2009
A new view of the tree of life Hug, Laura A.; Baker, Brett J.; Anantharaman, Karthik Nature Microbiology, Vol. 1, Issue 5 https://doi.org/10.1038/nmicrobiol.2016.48	journal	April 2016
Lipid analysis of CO2-rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria Probst, Alexander J.; Elling, Felix J.; Castelle, Cindy J. The ISME Journal, Vol. 14, Issue 6 https://doi.org/10.1038/s41396-020-0624-4	journal	March 2020
Assessing species biomass contributions in microbial communities via metaproteomics Kleiner, Manuel; Thorson, Erin; Sharp, Christine E. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01544-x	journal	November 2017
Muscle5: High-accuracy alignment ensembles enable unbiased assessments of sequence homology and phylogeny Edgar, Robert C. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-022-34630-w	journal	November 2022
Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface Probst, Alexander J.; Ladd, Bethany; Jarett, Jessica K. Nature Microbiology, Vol. 3, Issue 3 https://doi.org/10.1038/s41564-017-0098-y	journal	January 2018
The Effect of Microbial Induced Carbonate Precipitation on Fine-Grained Mine Tailings O’Toole, Conor; Liu, Qianwen; Montoya, Brina M. Geo-Congress 2022 https://doi.org/10.1061/9780784484012.035	conference	March 2022
Polysaccharide chemistry regulates kinetics of calcite nucleation through competition of interfacial energies Giuffre, Anthony J.; Hamm, Laura M.; Han, Nizhou Proceedings of the National Academy of Sciences, Vol. 110, Issue 23 https://doi.org/10.1073/pnas.1222162110	journal	May 2013
Mixotrophy in nanoflagellates across environmental gradients in the ocean Edwards, Kyle F. Proceedings of the National Academy of Sciences, Vol. 116, Issue 13 https://doi.org/10.1073/pnas.1814860116	journal	February 2019
The ATP/Substrate Stoichiometry of the ATP-binding Cassette (ABC) Transporter OpuA Patzlaff, Jason S.; van der Heide, Tiemen; Poolman, Bert Journal of Biological Chemistry, Vol. 278, Issue 32 https://doi.org/10.1074/jbc.M304796200	journal	May 2003
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses Capella-Gutierrez, S.; Silla-Martinez, J. M.; Gabaldon, T. Bioinformatics, Vol. 25, Issue 15 https://doi.org/10.1093/bioinformatics/btp348	journal	June 2009
MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph Li, Dinghua; Liu, Chi-Man; Luo, Ruibang Bioinformatics, Vol. 31, Issue 10 https://doi.org/10.1093/bioinformatics/btv033	journal	January 2015
GToTree: a user-friendly workflow for phylogenomics Lee, Michael D. Bioinformatics, Vol. 35, Issue 20 https://doi.org/10.1093/bioinformatics/btz188	journal	March 2019
GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database Chaumeil, Pierre-Alain; Mussig, Aaron J.; Hugenholtz, Philip Bioinformatics https://doi.org/10.1093/bioinformatics/btz848	journal	November 2019
The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences Perez-Riverol, Yasset; Bai, Jingwen; Bandla, Chakradhar Nucleic Acids Research, Vol. 50, Issue D1 https://doi.org/10.1093/nar/gkab1038	journal	November 2021
Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation Letunic, Ivica; Bork, Peer Nucleic Acids Research, Vol. 49, Issue W1 https://doi.org/10.1093/nar/gkab301	journal	April 2021
Carbon sequestration Lal, Rattan Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1492 https://doi.org/10.1098/rstb.2007.2185	journal	August 2007
Aggregatilinea lenta gen. nov., sp. nov., a slow-growing, facultatively anaerobic bacterium isolated from subseafloor sediment, and proposal of the new order Aggregatilineales ord. nov. within the class Anaerolineae of the phylum Chloroflexi Nakahara, Nozomi; Nobu, Masaru K.; Takaki, Yoshihiro International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 4 https://doi.org/10.1099/ijsem.0.003291	journal	April 2019
Whokaryote: distinguishing eukaryotic and prokaryotic contigs in metagenomes based on gene structure Pronk, Lotte J. U.; Medema, Marnix H. Microbial Genomics, Vol. 8, Issue 5 https://doi.org/10.1099/mgen.0.000823	journal	May 2022
Metals, minerals and microbes: geomicrobiology and bioremediation Gadd, G. M. Microbiology, Vol. 156, Issue 3 https://doi.org/10.1099/mic.0.037143-0	journal	December 2009
metaSPAdes: a new versatile metagenomic assembler Nurk, Sergey; Meleshko, Dmitry; Korobeynikov, Anton Genome Research, Vol. 27, Issue 5 https://doi.org/10.1101/gr.213959.116	journal	March 2017
Characterization of Melioribacter roseus gen. nov., sp. nov., a novel facultatively anaerobic thermophilic cellulolytic bacterium from the class Ignavibacteria , and a proposal of a novel bacterial phylum I gnavibacteriae Podosokorskaya, Olga A.; Kadnikov, Vitaly V.; Gavrilov, Sergey N. Environmental Microbiology, Vol. 15, Issue 6 https://doi.org/10.1111/1462-2920.12067	journal	January 2013
Metagenomic analysis of a high carbon dioxide subsurface microbial community populated by chemolithoautotrophs and bacteria and archaea from candidate phyla: High CO Emerson, Joanne B.; Thomas, Brian C.; Alvarez, Walter Environmental Microbiology, Vol. 18, Issue 6 https://doi.org/10.1111/1462-2920.12817	journal	April 2015
Comparison of DNA preservation methods for environmental bacterial community samples Gray, Michael A.; Pratte, Zoe A.; Kellogg, Christina A. FEMS Microbiology Ecology, Vol. 83, Issue 2 https://doi.org/10.1111/1574-6941.12008	journal	October 2012
Effects of environmental factors on microbial induced calcium carbonate precipitation: Environmental factors on MICP Mortensen, B. M.; Haber, M. J.; DeJong, J. T. Journal of Applied Microbiology, Vol. 111, Issue 2 https://doi.org/10.1111/j.1365-2672.2011.05065.x	journal	June 2011
Microbe-mineral interactions: early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas): Microbe-mineral interactions, Eleuthera Island, Bahamas Dupraz, C.; Visscher, P. T.; Baumgartner, L. K. Sedimentology, Vol. 51, Issue 4 https://doi.org/10.1111/j.1365-3091.2004.00649.x	journal	June 2004
Microbial diversity in modern marine stromatolites, Highborne Cay, Bahamas Baumgartner, Laura K.; Spear, John R.; Buckley, Daniel H. Environmental Microbiology, Vol. 11, Issue 10 https://doi.org/10.1111/j.1462-2920.2009.01998.x	journal	October 2009
A likely role for anoxygenic photosynthetic microbes in the formation of ancient stromatolites Bosak, T.; Greene, S. E.; Newman, D. K. Geobiology, Vol. 5, Issue 2 https://doi.org/10.1111/j.1472-4669.2007.00104.x	journal	April 2007
Inside the alkalinity engine: the role of electron donors in the organomineralization potential of sulfate-reducing bacteria Gallagher, K. L.; Kading, T. J.; Braissant, O. Geobiology, Vol. 10, Issue 6 https://doi.org/10.1111/j.1472-4669.2012.00342.x	journal	August 2012
Cool water geyser travertine: Crystal Geyser, Utah, USA Barth, Jennifer A.; Chafetz, Henry S. Sedimentology, Vol. 62, Issue 3 https://doi.org/10.1111/sed.12158	journal	October 2014
The Maltodextrin System ofEscherichia coli: Metabolism and Transport Dippel, Renate; Boos, Winfried Journal of Bacteriology, Vol. 187, Issue 24 https://doi.org/10.1128/JB.187.24.8322-8331.2005	journal	December 2005
Structure, Function, and Evolution of Bacterial ATP-Binding Cassette Systems Davidson, A. L.; Dassa, E.; Orelle, C. Microbiology and Molecular Biology Reviews, Vol. 72, Issue 2 https://doi.org/10.1128/MMBR.00031-07	journal	June 2008
Evaluation of RNA later as a Field-Compatible Preservation Method for Metaproteomic Analyses of Bacterium-Animal Symbioses Jensen, Marlene; Wippler, Juliane; Kleiner, Manuel Microbiology Spectrum, Vol. 9, Issue 2 https://doi.org/10.1128/Spectrum.01429-21	journal	October 2021
phyloFlash: Rapid Small-Subunit rRNA Profiling and Targeted Assembly from Metagenomes Gruber-Vodicka, Harald R.; Seah, Brandon K. B.; Pruesse, Elmar mSystems, Vol. 5, Issue 5 https://doi.org/10.1128/mSystems.00920-20	journal	October 2020
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Microbial mats in the Turks and Caicos Islands reveal diversity and evolution of phototrophy in the Chloroflexota order Aggregatilineales Ward, Lewis M.; Lingappa, Usha F.; Grotzinger, John P. Environmental Microbiome, Vol. 15, Issue 1 https://doi.org/10.1186/s40793-020-00357-8	journal	April 2020
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P. PLoS ONE, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pone.0009490	journal	March 2010
On the Strategy of "Eating Your Competitor": A Mathematical Analysis of Algal Mixotrophy Thingstad, T. Frede; Havskum, Harry; Garde, Kristine Ecology, Vol. 77, Issue 7 https://doi.org/10.2307/2265705	journal	October 1996
Carbonate Precipitation through Microbial Activities in Natural Environment, and Their Potential in Biotechnology: A Review Zhu, Tingting; Dittrich, Maria Frontiers in Bioengineering and Biotechnology, Vol. 4 https://doi.org/10.3389/fbioe.2016.00004	journal	January 2016
Home-Made Cost Effective Preservation Buffer Is a Better Alternative to Commercial Preservation Methods for Microbiome Research Menke, Sebastian; Gillingham, Mark A. F.; Wilhelm, Kerstin Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00102	journal	January 2017
Key Role of Alphaproteobacteria and Cyanobacteria in the Formation of Stromatolites of Lake Dziani Dzaha (Mayotte, Western Indian Ocean) Gérard, Emmanuelle; De Goeyse, Siham; Hugoni, Mylène Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00796	journal	May 2018
Can Microbially Induced Calcite Precipitation (MICP) through a Ureolytic Pathway Be Successfully Applied for Removing Heavy Metals from Wastewaters? Torres-Aravena, Álvaro Esteban; Duarte-Nass, Carla; Azócar, Laura Crystals, Vol. 8, Issue 11 https://doi.org/10.3390/cryst8110438	journal	November 2018
Biomineralization Induced by Cells of Sporosarcina pasteurii: Mechanisms, Applications and Challenges Wu, Yang; Li, Huimin; Li, Yang Microorganisms, Vol. 9, Issue 11 https://doi.org/10.3390/microorganisms9112396	journal	November 2021
Cyanobacteria as Biocatalysts for Carbonate Mineralization Kamennaya, Nina; Ajo-Franklin, Caroline; Northen, Trent Minerals, Vol. 2, Issue 4 https://doi.org/10.3390/min2040338	journal	October 2012
Nitrogen and oxygen isotope fractionation during dissimilatory nitrate reduction by denitrifying bacteria Granger, Julie; Sigman, Daniel M.; Lehmann, Moritz F. Limnology and Oceanography, Vol. 53, Issue 6 https://doi.org/10.4319/lo.2008.53.6.2533	journal	November 2008

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