Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer

ISME Journal

Volumn 8, Issue 7, 2014, Pages 1452-1463

  Wrighton, Kelly C ^a   Castelle, Cindy J ^b   Wilkins, Michael J ^a   Hug, Laura A ^b   Sharon, Itai ^b   Thomas, Brian C ^b   Handley, Kim M ^c   Mullin, Sean W ^b   Nicora, Carrie D ^d   Singh, Andrea ^b   Lipton, Mary S ^d   Long, Philip E ^e   Williams, Kenneth H ^e   Banfield, Jillian F ^b,d  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^e LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

candidate phylum; fermentation; hydrogenase; metagenomics; microbial diversity; proteomics; sulfate reduction

Indexed keywords

FERMENTATION; GENOMICS; MICROBIAL COMMUNITY; NUTRIENT CYCLING; ORGANIC CARBON; PHYLOGENETICS; PROTEOMICS; RESPIRATION; SULFATE; TAXONOMY; UNCONFINED AQUIFER;

COLORADO; COLORADO RIVER [NORTH AMERICA]; RIFLE; UNITED STATES;

BACTEROIDALES; CHLOROFLEXI; CHLOROFLEXI (CLASS); CYANOBACTERIA; MAMMALIA; PROTEOBACTERIA;

CARBON; GROUND WATER; HYDROGEN; HYDROGENASE; IRON; NITROGEN; SULFUR;

AEROBIC METABOLISM; ARTICLE; BACTEROIDETES; CHEMISTRY; CHLOROFLEXI; CLASSIFICATION; ECOSYSTEM; FERMENTATION; GENETICS; METABOLISM; METAGENOMICS; MICROBIOLOGY; PHYLOGENY; PROTEOBACTERIA; PROTEOMICS;

AEROBIOSIS; BACTEROIDETES; CARBON; CHLOROFLEXI; ECOSYSTEM; FERMENTATION; GROUNDWATER; HYDROGEN; HYDROGENASE; IRON; METAGENOMICS; NITROGEN; PHYLOGENY; PROTEOBACTERIA; PROTEOMICS; SULFUR;

EID: 84903395728     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.249     Document Type: Article

References (56)

1. Aklujkar M, Young ND, Holmes D, Chavan M, Risso C, Kiss HE et al. (2010). The genome of Geobacter bemidjiensis, exemplar for the subsurface clade of Geobacter species that predominate in Fe(III)-reducing subsurface environments. BMC Genomics 11: 490
2. Allgaier M, Reddy A, Park JI, Ivanova N, D'haeseleer P, Lowry S et al. (2010). Targeted discovery of glycoside hydrolases from a switchgrass-Adapted compost community. PLoS One 5: E8812
3. Averill BA. (1996). Dissimilatory nitrite and nitric oxide reductases. Chem Rev 96: 2951-2964
4. Ballor NR, Leadbetter Jr. (2011). Analysis of extensive [FeFe] hydrogenase gene diversity within the gut microbiota of insects representing five families of Dictyoptera. Microbial Ecol 63: 586-595
5. Beller HR, Chain PS, Letain TE, Chakicherla A, Larimer FW, Richardson PM et al. (2006). The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol 188: 1473-1488. (Pubitemid 43228681
6. Berlemont R, Martiny AC. (2013). Phylogenetic distribution of potential cellulases in bacteria. Appl Environ Microbiol 79: 1545-1554
7. Bianchi TS. (2011). The role of terrestrially derived organic carbon in the coastal ocean: A changing paradigm and the priming effect. Proc Natl Acad Sci 108: 19473-19481
8. Brazelton WJ, Nelson B, Schrenk MO. (2012). Metagenomic evidence for H2 oxidation and H2 production by serpentinite-hosted subsurface microbial communities. Front Microbiol 2: 268
9. Briée C, Moreira D, López-García P. (2007). Archaeal and bacterial community composition of sediment and plankton from a suboxic freshwater pond. Res Microbiol 158: 213-227
10. Byrne-Bailey KG, Weber KA, Chair AH, Bose S, Knox T, Spanbauer TL et al. (2010). Completed genome sequence of the anaerobic iron-oxidizing bacterium Acidovorax ebreus strain TPSY. J Bacteriol 192: 1475-1476
11. Castelle CJ, Hug LA, Wrighton KC, Thomas BC, Williams KH, Wu D et al. (2013). Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. Nat Commun 4: 2120
12. Coates JD, Chakraborty R, Lack JG, O'Connor SM, Cole KA, Bender KS et al. (2001). Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411: 1039-1043. (Pubitemid 32612326
13. Dick GJ, Andersson AF, Baker BJ, Simmons SL, Thomas BC, Yelton AP et al. (2009). Community-wide analysis of microbial genome sequence signatures. Genome Biol 10: R85
14. Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA, Thomas BC et al.The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife (2013). 2: E01102
15. Druhan JL, Steefel CI, Molins S, Williams KH, Conrad ME, DePaolo DJ. (2012). Timing the onset of sulfate reduction over multiple subsurface acetate amendments by measurement and modeling of sulfur isotope fractionation. Environ Sci Technol 46: 8895-8902
16. Engelhardt T, Sahlberg M, Cypionka H, Engelen B. (2011). Induction of prophages from deep-subseafloor bacteria. Environ Microbiol 3: 459-465
17. Finster K, Liesack W, Thamdrup B. (1998). Elemental sulfur and thiosulfate disproportionation by Desulfocapsa sulfoexigens sp. nov., a new anaerobic bacterium isolated from marine surface sediment. Appl Environ Microbiol 64: 119-125. (Pubitemid 28040301
18. Friedrich CG, Rother D, Bardischewksy F, Quentmeier A, Fischer J. (2001). Oxidation of reduced inorganic sulfur compounds by bacteria: Emergence of a common mechanism? Appl Environ Microbiol 67: 2873-2882
19. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P, Tiedje JM. (2007). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Systemic Evolutionary Microbiol 57: 81-91. (Pubitemid 46152735
20. Grant RF, Desai AR, Sulman BN. (2012). Modelling contrasting responses of wetland productivity to changes in water table depth. Biogeosciences Discussions 9: 5579-5623
21. Green SJ, Prakash O, Gihring TM, Akob DM, Jasrotia P, Jardine PM et al. (2010). Denitrifying Bacteria isolated from terrestrial subsurface sediments exposed to mixed-waste contamination. Appl Environ Microbiol 76: 3244-3254
22. Handley KM, VerBerkmoes NC, Steefel CI, Williams KH, Sharon I, Miller CS et al. (2013). Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community. ISME J 7: 800-816
23. Handley KM, Wrighton KC, Piceno YM, Andersen GL, DeSantis TZ, Williams KH et al. (2012). High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment. FEMS Microbiol Ecol 81: 188-204
24. Herrmann G, Jayamani E, Mai G, Buckel W. (2008). Energy conservation via electron-Transferring flavoprotein in anaerobic bacteria. J Bacteriol 190: 784-791. (Pubitemid 351170920
25. Hug LA, Castelle CJ, Wrighton KC, Thomas BC, Sharon I, Frischkorn KR et al. (2013). Community genomic analyses constrain the distribution of metabolic traits across the Chloroflexi phylum and indicate roles in sediment carbon cycling. Microbiome 1: 22
26. Kantor RS, Wrighton KC, Handley KM, Sharon I, Hug LA, Castelle CJ et al. (2013). Small genomes and sparse metabolisms of sediment-Associated bacteria from four candidate phyla. mBio 4: E00708-e00713
27. Knoblauch C, Sahm K, Jørgensen BB. (1999). Psychrophilic sulfate-reducing bacteria isolated from permanently cold arctic marine sediments: Description of Desulfofrigus oceanense gen. nov., sp. nov., Desulfofrigus fragile sp. nov., Desulfofaba gelida gen. nov., sp. nov., Desulfotalea psychrophila gen. nov., sp. nov. and Desulfotalea arctica sp. nov. Int J Syst Bacteriol 49: 1631-1643. (Pubitemid 29519095
28. Kuzyakov Y, Friedel JK, Stahr K. (2000). Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32: 1485-1498
29. Miletto M, Williams KH, N'Guessan AL, Lovley DR. (2011). Molecular analysis of the metabolic rates of discrete subsurface populations of sulfate reducers. Appl Environ Microbiol 77: 6502-6509
30. Pereira IA, LeGall J, Xavier AV, Teixeira M. (2000). Characterization of a heme c nitrite reductase from a non-Ammonifying microorganism, Desulfovibrio vulgaris Hildenborough. Biochimica et Biophysica Acta 1481: 119-130. (Pubitemid 30658088
31. Peura S, Eiler A, Bertilsson S, Tiirola M, Jones RI. (2012). Distinct and diverse anaerobic bacterial communities in boreal lakes dominated by candidate division OD1. ISME J 1-13
32. Raes J, Korbel JO, Lercher MJ, Mering VC, Bork P. (2007). Prediction of effective genome size in metagenomic samples. Genome Biol 8: 1
33. Rabus R, Ruepp A, Frickey T, Rattei T, Fartmann B, Stark M et al. (2004). The genome of Desulfotalea psychrophila, a sulfate-reducing bacterium from permanently cold Arctic sediments. Environm Microbiol 6: 887-902. (Pubitemid 39123243
34. Riley WJ, Subin ZM, Lawrence DM, Swenson SC, Torn MS, Meng L et al. (2011). Barriers to predicting changes in global terrestrial methane fluxes: Analyses using CLM4Me, a methane biogeochemistry model integrated in CESM. Biogeosciences 8: 1925-1953
35. Rivett MO, Buss SR, Morgan P, Smith JWN, Bemment CD. (2008). Nitrate attenuation in groundwater: A review of biogeochemical controlling processes. Water Res 42: 4215-4232
36. Roychoudhury AN, Merrett GL. (2006). Redox pathways in a petroleum contaminated shallow sandy aquifer: Iron and sulfate reductions. Sci Total Environ 366: 262-274
37. Schmidt O, Drake HL, Horn MA. (2010). Hitherto unknown [Fe-Fe]-hydrogenase gene diversity in anaerobes and anoxic enrichments from a moderately acidic fen. Appl Environ Microbiol 76: 2027-2031
38. Schut GJ, Adams MWW. (2009). The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: A new perspective on anaerobic hydrogen production. J Bacteriol 191: 4451-4457
39. Sharma S, Cavallaro G, Rosato A. (2010). A systematic investigation of multiheme c-Type cytochromes in prokaryotes. J Biol Inorganic Chem 15: 559-571
40. Sharon I, Morowitz MJ, Thomas BC, Costello EK, Relman DA, Banfield JF. (2013). Time series community genomics analysis reveals rapid shifts in bacterial species, strains, and phage during infant gut colonization. Genome Res 23: 111-120
41. Shrout JD, Scheetz TE, Casavant TL, Parkin GF. (2005). Isolation and characterization of autotrophic, hydrogen-utilizing, perchlorate-reducing bacteria. Appl Microbiol Biotechnol 67: 261-268. (Pubitemid 40591279
42. Sieber JR, McInerney MJ, Gunsalus RP. (2012). Genomic insights into syntrophy: The paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66: 429-452
43. Thamdrup B, Finster K, Wurgler Hansen J, Bak F. (1993). Bacterial disproportionation of elemental sulfur coupled to chemical reduction of iron or manganese. Appl Environ Microbiol 59: 101-108
44. Tveit A, Schwacke R, Svenning MM, Urich T. (2013). Organic carbon transformation in high-Arctic peat soils: Key functions and microorganisms. ISME J 7: 299-311
45. Vignais PM, Billoud B. (2007). Occurrence, classification, and biological function of hydrogenases: An overview. Chem Rev 107: 4206-4272. (Pubitemid 350041744
46. Weber KA, Achenbach LA, Coates JD. (2006). Microorganisms pumping iron: Anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4: 752-764. (Pubitemid 44420126
47. Whitman WB, Coleman DC, Wiebe WJ. (1998). Prokaryotes: The unseen majority. Proc Natl Acad Sci USA 95: 6578-6583. (Pubitemid 28278022
48. Wilkins MJ, Callister SJ, Miletto M, Williams KH, Nicora CD, Lovley DR et al. (2010). Development of a biomarker for Geobacter activity and strain composition; Proteogenomic analysis of the citrate synthase protein during bioremediation of U(VI). Microbial Biotechnol 4: 55-63
49. Wilkins MJ, Wrighton KC, Nicora CD, Williams KH, McCue LA, Handley KM et al. (2013). Fluctuations in species-level protein expression occur during element and nutrient cycling in the subsurface. PLoS One 8: E57819
50. Williams KH, Long PE, Davis JA, Wilkins MJ, N'Guessan AL, Steefel CI et al. (2011). Acetate availability and its influence on sustainable bioremediation of uranium-contaminated groundwater. Geomicrobiol J 28: 519-539
51. Wrighton KC, Thomas BC, Sharon I, Miller CS, Castelle CJ, VerBerkmoes NC et al. (2012). Fermentation, hydrogen, and sulfur metabolism in multiple uncultivated bacterial phyla. Science 337: 1661-1665
52. Wrighton KC, Thrash JC, Melnyk RA, Bigi JP, Byrne-Bailey KG, Remis JP et al. (2011). Evidence for direct electron transfer by a Gram-positive bacterium isolated from a microbial fuel cell. Appl Environ Microbiol 77: 7633-7639
53. Yabusaki SB, Fang Y, Williams KH, Murray CJ, Ward AL, Dayvault RD et al. (2011). Variably saturated flow and multicomponent biogeochemical reactive transport modeling of a uranium bioremediation field experiment. J Contaminant Hydrol 126: 271-290
54. Yamada T, Sekiguchi Y, Hanada S, Imachi H, Ohashi A, Harada H et al. (2006). Anaerolinea thermolimosa sp. nov, Levilinea saccharolytica gen. nov., sp. nov. and Leptolinea tardivitalis gen. nov., sp. nov., novel filamentous anaerobes, and description of the new classes Anaerolineae classis nov. and Caldilineae classis nov. in the bacterial phylum Chloroflexi. Int J Syst Evolutionary Microbiol 56: 1331-1340. (Pubitemid 43933829
55. Zehr JP, Jenkins BD, Short SM, Steward GF. (2003). Nitrogenase gene diversity and microbial community structure: A cross-system comparison. Environ Microbiol 5: 539-554. (Pubitemid 36832210
56. Zhuang K, Izallalen M, Mouser P, Richter H, Risso C, Mahadevan R et al. (2010). Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J 5: 305-316