Abstract
Diverse microbial communities living in subsurface coal seams are responsible for important geochemical processes including the movement of carbon between the geosphere, biosphere and atmosphere. Microbial conversion of the organic matter in coal to methane involves a complex assemblage of bacteria and archaea working in syntrophic relationships. Despite the importance and value of this microbial process, very few of the microbial taxa have defined metabolic or ecological roles in these environments. Additionally, the genomic features mediating life in this chemically reduced, energy poor, deep subsurface environment are not well characterised. Here we describe the isolation and genomic and catabolic characterisation of three alphaproteobacterial Stappia indica species from three coal basins across Australia. S. indica genomes from coal seams were compared with those from closely related S. indica isolated from diverse surface waters, revealing a coal seam-specific suite of genes associated with life in the subsurface. These genes are linked to processes including viral defence, secondary metabolite production, polyamine metabolism, polypeptide uptake membrane transporters and putative energy neutral pressure-dependent CO2 fixation. This indicates that subsurface Stappia have diverse metabolisms for biomass recycling and pressure-dependent CO2 fixation and require a suite of defensive and competitive strategies relative to their surface-dwelling relatives.
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Strąpoć D, Mastalerz M, Dawson K, Macalady J, Callaghan AV, Wawrik B, Turich C, Ashby M (2011) Biogeochemistry of microbial coal-bed methane. Annu Rev Earth Planet Sci 39:617–656
Rabl A, Spadaro JV (2006) Environmental impacts and costs of energy. Ann N Y Acad Sci 1076:516–526
Markandya A, Wilkinson P (2007) Electricity generation and health. Lancet 370:979–990
Faiz M, Hendry P (2006) Significance of microbial activity in Australian coal bed methane reservoirs—a review. Bull Can Petrol Geol 54:261–272
Barnhart EP, Weeks EP, Jones EJP, Ritter DJ, McIntosh JC, Clark AC, Ruppert LF, Cunningham AB, Vinson DS, Orem W, Fields MW (2016) Hydrogeochemistry and coal-associated bacterial populations from a methanogenic coal bed. Int J Coal Geol 162:14–26
Meslé M, Dromart G, Oger P (2013) Microbial methanogenesis in subsurface oil and coal. Res Microbiol 164:959–972
Colosimo F, Thomas R, Lloyd JR, Taylor KG, Boothman C, Smith AD, Lord R, Kalin RM (2016) Biogenic methane in shale gas and coal bed methane: a review of current knowledge and gaps. Int J Coal Geol 165:106–120
Ritter D, Vinson D, Barnhart E, Akob DM, Fields MW, Cunningham AB, Orem W, McIntosh JC (2015) Enhanced microbial coalbed methane generation: a review of research, commercial activity, and remaining challenges. Int J Coal Geol 146:28–41
Vick SH, Greenfield P, Tran-Dinh N, Tetu SG, Midgley DJ, Paulsen IT (2018) The coal seam microbiome (CSMB) reference set, a lingua franca for the microbial coal-to-methane community. Int J Coal Geol 186:41–50
Liu Y, Whitman WB (2008) Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea. Ann N Y Acad Sci 1125:171–189
Vick SH, Gong S, Sestak S, Vergara TJ, Pinetown KL, Li Z, Greenfield P, Tetu SG, Midgley DJ, Paulsen IT (2019) Who eats what? Unravelling microbial conversion of coal to methane. FEMS Microbiol Ecol 95:fiz093
Barnhart EP, Davis KJ, Varonka M, Orem W, Cunningham AB, Ramsay BD, Fields MW (2017) Enhanced coal-dependent methanogenesis coupled with algal biofuels: potential water recycle and carbon capture. Int J Coal Geol 171:69–75
Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12:259–276
Vick SH, Greenfield P, Pinetown KL, Sherwood N, Gong S, Tetu SG, Midgley DJ, Paulsen IT (2019) Succession patterns and physical niche partitioning in microbial communities from subsurface coal seams. iScience 12:152–167
Pujalte MJ, Lucena T, Ruvira MA, Arahal DR, Macián MC (2014) The family Rhodobacteraceae. In: Roseberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, Heidelberg, pp 439–512
Weber CF, King GM (2007) Physiological, ecological, and phylogenetic characterization of Stappia, a marine CO-oxidizing bacterial genus. Appl Environ Microbiol 73:1266–1276
Kim B-C, Park JR, Bae J-W, Rhee S-K, Kim K-H, Oh J-W, Park Y-H (2006) Stappia marina sp. nov., a marine bacterium isolated from the Yellow Sea. Int J Syst Evol Microbiol 56:75–79
Rüger H-J, Höfle MG (1992) Marine star-shaped-aggregate-forming bacteria: Agrobacterium atlanticum sp. nov.; Agrobacterium meteori sp. nov.; Agrobacterium ferrugineum sp. nov., nom. rev.; Agrobacterium gelatinovorum sp. nov., nom. rev.; and Agrobacterium stellulatum sp. nov., nom. rev. Int J Syst Evol Microbiol 42:133–143
Groben R, Doucette GJ, Kopp M, Kodama M, Amann R, Medlin LK (2000) 16S rRNA targeted probes for the identification of bacterial strains isolated from cultures of the toxic dinoflagellate Alexandrium tamarense. Microb Ecol 39:186–196
Pujalte MJ, Macián MC, Arahal DR, Garay E (2005) Stappia alba sp. nov., isolated from Mediterranean oysters. Syst Appl Microbiol 28:672–678
Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P, Lopez J (2005) A molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 28:242–264
Greenfield P, Duesing K, Papanicolaou A, Bauer DC (2014) Blue: correcting sequencing errors using consensus and context. Bioinformatics 30:2723–2732
Zerbino DR, Birney E (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18:821–829
Markowitz VM, Chen I-MA, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P (2012) IMG: the integrated microbial genomes database and comparative analysis system. Nucleic Acids Res 40:D115–D122
Henao J, Pérez H, Abril D, Ospina K, Piza A, Botero K, et al. (2017). Genome sequencing of three bacteria associated to black band disease from a Colombian reef-building coral. Genomics data 11: 73–74
Díaz-Cárdenas C, Baena S (2015). Manantiales salinos: Inventarios de Diversidad Metabólica y filogenética de microorganismos de ambientes salinos. Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales 39: 358–373
Tully BJ, Graham ED, Heidelberg JF (2018) The reconstruction of 2,631 draft metagenome-assembled genomes from the global oceans. Scientific data 5: 170203
Donachie SP, Bowman JP, Alam M (2006) Nesiotobacter exalbescens gen. nov., sp. nov., a moderately thermophilic alphaproteobacterium from an Hawaiian hypersaline lake. Int J Syst Evol Microbiol 56: 563–567
Wang M, Zhang X, Jiang T, Hu S, Yi Z, Zhou Y, et al. (2017) Liver abscess caused by Pannonibacter phragmitetus: Case report and literature review. Frontiers in medicine 4: 48
Li S-G, Tang Y-Q, Nie Y, Cai M, Wu X-L (2011) Complete genome sequence of Polymorphum gilvum SL003B-26A1T, a crude oil-degrading bacterium from oil-polluted saline soil. J Bacteriol 193: 2894–2895
Xu Y, Li Q, Tian R, Lai Q, Zhang Y (2015). Pseudovibrio hongkongensis sp. nov., isolated from a marine flatworm. Antonie Van Leeuwenhoek 108: 127-132
Simon M, Scheuner C, Meier-Kolthoff JP, Brinkhoff T, Wagner-Döbler I, Ulbrich M, Klenk H-P, Schomburg D, Petersen J, Göker M (2017) Phylogenomics of Rhodobacteraceae reveals evolutionary adaptation to marine and non-marine habitats. The ISME journal 11:1483–1499
Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069
Lechner M, Findeiß S, Steiner L, Marz M, Stadler PF, Prohaska SJ (2011) Proteinortho: detection of (co-) orthologs in large-scale analysis. BMC Bioinformatics 12:124
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard J-F, Guindon S, Lefort V, Lescot M (2008) Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36:W465–W469
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
Chevenet F, Brun C, Bañuls A-L, Jacq B, Christen R (2006) TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformatics 7:439
Sutcliffe B, Chariton AA, Harford AJ, Hose GC, Stephenson S, Greenfield P, Midgley DJ, Paulsen IT (2018) Insights from the genomes of microbes thriving in uranium-enriched sediments. Microb Ecol 75:970–984
Boc A, Diallo AB, Makarenkov V (2012) T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res 40:W573–W579
Svd W, Colbert SC, Varoquaux G (2011) The NumPy array: a structure for efficient numerical computation. Comput Sci Eng 13:22–30
Hunter JD (2007) Matplotlib: a 2D graphics environment. Comput Sci Eng 9:90–95
Pedregosa F, Varoquaux G, Gramfort A, Michel V, Thirion B, Grisel O, Blondel M, Prettenhofer P, Weiss R, Dubourg V (2011) Scikit-learn: machine learning in python. J Mach Learn Res 12:2825–2830
Kanehisa M, Sato Y, Morishima K (2016) BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 428:726–731
Elbourne LD, Tetu SG, Hassan KA, Paulsen IT (2017) TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res 45:D320–D324
Yin Y, Mao X, Yang J, Chen X, Mao F, Xu Y (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40:W445–W451
Grissa I, Vergnaud G, Pourcel C (2007) CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res 35:W52–W57
Weber T, Blin K, Duddela S, Krug D, Kim HU, Bruccoleri R, Lee SY, Fischbach MA, Müller R, Wohlleben W (2015) antiSMASH 3.0—a comprehensive resource for the genome mining of biosynthetic gene clusters. Nucleic Acids Res 43:W237–W243
Varani AM, Siguier P, Gourbeyre E, Charneau V, Chandler M (2011) ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes. Genome Biol 12:R30
Vick SH, Greenfield P, Pinetown KL, Sherwood N, Gong S, Tetu SG, Midgley DJ, Paulsen IT (2019) Patterns of succession and physical niche partitioning in coal associated microbial communities from the terrestrial subsurface. iScience
An D, Caffrey SM, Soh J, Agrawal A, Brown D, Budwill K, Dong X, Dunfield PF, Foght J, Gieg LM (2013) Metagenomics of hydrocarbon resource environments indicates aerobic taxa and genes to be unexpectedly common. Environ Sci Technol 47:10708–10717
Zhu H, Chang M, Wang H (2017) Study on primal CO gas generation and emission of coal seam. Int J Min Sci Technol 27:973–979
Wang L, Nie Y, Tang Y-Q, Song X-M, Cao K, Sun L-Z, Wang Z-J, Wu X-L (2016) Diverse bacteria with lignin degrading potentials isolated from two ranks of coal. Front Microbiol 7:1428
Singh DN, Tripathi AK (2013) Coal induced production of a rhamnolipid biosurfactant by Pseudomonas stutzeri, isolated from the formation water of Jharia coalbed. Bioresour Technol 128:215–221
Singh DN, Tripathi AK (2011) Evaluation of the coal-degrading ability of Rhizobium and Chelatococcus strains isolated from the formation water of an Indian coal bed. J Microbiol Biotechnol 21:1101–1108
Cohan FM (2002) What are bacterial species? Annu Rev Microbiol 56:457–487
Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science 323:741–746
Williams KP, Sobral BW, Dickerman AW (2007) A robust species tree for the alphaproteobacteria. J Bacteriol 189:4578–4586
Petersen J, Brinkmann H, Pradella S (2009) Diversity and evolution of repABC type plasmids in Rhodobacterales. Environ Microbiol 11:2627–2638
Abe F (2007) Exploration of the effects of high hydrostatic pressure on microbial growth, physiology and survival: perspectives from piezophysiology. Biosci Biotechnol Biochem 71:2347–2357
Abe F, Horikoshi K (2001) The biotechnological potential of piezophiles. Trends Biotechnol 19:102–108
Yayanos AA (2001) Barophiles and piezophiles. John Wiley & Sons, Ltd, Chichester
Eisenmenger MJ, Reyes-De-Corcuera JI (2009) High pressure enhancement of enzymes: a review. Enzym Microb Technol 45:331–347
Windle CD, Perutz RN (2012) Advances in molecular photocatalytic and electrocatalytic CO2 reduction. Coord Chem Rev 256:2562–2570
Wiebe R, Gaddy V (1940) The solubility of carbon dioxide in water at various temperatures from 12 to 40 and at pressures to 500 atmospheres. Critical phenomena. J Am Chem Soc 62:815–817
Baranenko V, Kirov V (1989) Solubility of hydrogen in water in a broad temperature and pressure range. Sov At Energy 66:30–34
Ji M, Greening C, Vanwonterghem I, Carere CR, Bay SK, Steen JA, Montgomery K, Lines T, Beardall J, van Dorst J (2017) Atmospheric trace gases support primary production in Antarctic desert surface soil. Nature 552:400–403
Wortham BW, Oliveira MA, Patel CN (2007) Polyamines in bacteria: pleiotropic effects yet specific mechanisms. In: Perry RD, Fetherston JD (eds) The genus Yersinia advances in experimental medicine and biology. Springer, New York, pp 106–115
Takatsuka Y, Kamio Y (2004) Molecular dissection of the Selenomonas ruminantium cell envelope and lysine decarboxylase involved in the biosynthesis of a polyamine covalently linked to the cell wall peptidoglycan layer. Biosci Biotechnol Biochem 68:1–19
Daly RA, Borton MA, Wilkins MJ, Hoyt DW, Kountz DJ, Wolfe RA, Welch SA, Marcus DN, Trexler RV, MacRae JD (2016) Microbial metabolisms in a 2.5-km-deep ecosystem created by hydraulic fracturing in shales. Nat Microbiol 1:16146
Hammerschmidt S, Hilse R, Van Putten J, Gerardy-Schahn R, Unkmeir A, Frosch M (1996) Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J 15:192–198
Ziebuhr W, Krimmer V, Rachid S, Lößner I, Götz F, Hacker J (1999) A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol 32:345–356
Acknowledgements
The authors would like to thank the Macquarie University Microscopy department, in particular Dr. Sue Lindsay, Dr. Nadia Suarez-Bosche and Ms. Nicole Vella, for their assistance and guidance in generating scanning electron micrographs.
Funding
Mr. Silas Vick was supported by a Macquarie University funded postgraduate scholarship. This work was supported by a CSIRO Energy strategic research initiative.
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Vick, S.H.W., Greenfield, P., Willows, R.D. et al. Subsurface Stappia: Success Through Defence, Specialisation and Putative Pressure-Dependent Carbon Fixation. Microb Ecol 80, 34–46 (2020). https://doi.org/10.1007/s00248-019-01471-y
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DOI: https://doi.org/10.1007/s00248-019-01471-y