Vitamin and amino acid auxotrophy in anaerobic consortia operating under methanogenic conditions

mSystems

Volumn 2, Issue 5, 2017, Pages

  Hubalek, Valerie ^a,b   Buck, Moritz ^a,c   Tan, Boonfei ^d,e   Foght, Julia ^d   Wendeberg, Annelie ^f   Berry, David ^g   Bertilsson, Stefan ^a   Eilera, Alexander ^a,h  

^a UPPSALA UNIVERSITY   (Sweden)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c NBIS   (Sweden)

^d UNIVERSITY OF ALBERTA   (Canada)

^e SINGAPORE MIT ALLIANCE FOR RESEARCH AND TECHNOLOGY   (Singapore)

^f HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^g UNIVERSITY OF VIENNA   (Austria)

^h eDNA solutions Ltd   (Sweden)

Author keywords

Black Queen hypothesis; Metagenomics; Petroleum; Syntrophy

Indexed keywords

EID: 85041493448     PISSN: None     EISSN: 23795077     Source Type: Journal    
DOI: 10.1128/mSystems.00038-17     Document Type: Article

References (65)

1. Head IM, Jones DM, Larter SR. 2003. Biological activity in the deep subsurface and the origin of heavy oil. Nature 426:344 -352. https://doi .org/10.1038/nature02134.
2. Gray ND, Sherry A, Hubert C, Dolfing J, Head IM. 2010. Methanogenic degradation of petroleum hydrocarbons in subsurface environments remediation, heavy oil formation, and energy recovery. Adv Appl Microbiol 72:137-161. http://www.sciencedirect.com/science/article/pii/ S0065216410720050. https://doi.org/10.1016/S0065-2164(10)72005-0.
3. Berdugo-Clavijo C, Dong X, Soh J, Sensen CW, Gieg LM. 2012. Methanogenic biodegradation of two-ringed polycyclic aromatic hydrocarbons. FEMS Microbiol Ecol 81:124 -133. http://femsec.oxfordjournals .org/content/81/1/124.abstract. https://doi.org/10.1111/j.1574-6941 .2012.01328.x.
4. Leahy JG, Colwell RR. 1990. Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305-315. http://www.ncbi.nlm.nih .gov/pmc/articles/PMC372779/.
5. Quagraine EK, Peterson HG, Headley JV. 2005. In situ bioremediation of naphthenic acids contaminated tailing pond waters in the Athabasca oil sands region-demonstrated field studies and plausible options: A review. J Environ Sci Health A Tox Hazard Subst Environ Eng 40:685-722. https://doi.org/10.1081/ESE-200046649.
6. Kelly EN, Short JW, Schindler DW, Hodson PV, Ma M, Kwan AK, Fortin BL. 2009. Oil sands development contributes polycyclic aromatic compounds to the Athabasca River and its tributaries. Proc Natl Acad Sci U S A 106:22346-22351. http://www.pnas.org/content/106/52/22346 .abstract. https://doi.org/10.1073/pnas.0912050106.
7. Kelly EN, Schindler DW, Hodson PV, Short JW, Radmanovich R, Nielsen CC. 2010. Oil sands development contributes elements toxic at low concentrations to the Athabasca River and its tributaries. Proc Natl Acad Sci U S A 107:16178-16183. http://www.pnas.org/content/107/37/16178 .abstract. https://doi.org/10.1073/pnas.1008754107.
8. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (ed). 2007. The physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom.
9. Schink B. 1985. Degradation of unsaturated hydrocarbons by methanogenic enrichment cultures. FEMS Microbiol Ecol 1:69 -77. https://doi.org/ 10.1111/j.1574-6968.1985.tb01133.x.
10. Zengler K, Richnow HH, Rossello-Mora R, Michaelis W, Widdel F. 1999. Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266 -269. https://doi.org/10.1038/45777.
11. Wang L-Y, Gao C-X, Mbadinga SM, Zhou L, Liu J-F, Gu J-D, Mu B-Z. 2011. Characterization of an alkane-degrading methanogenic enrichment culture from production water of an oil reservoir after 274 days of incubation. Int Biodeterior Biodegrad 65:444-450. http://www.sciencedirect .com/science/article/pii/S0964830511000138. https://doi.org/10.1016/j .ibiod.2010.12.010.
12. Tan B, Dong X, Sensen CW, Foght J. 2013. Metagenomic analysis of an anaerobic alkane-degrading microbial culture: Potential hydrocarbonactivating pathways and inferred roles of community members. Genome 56:599-611. https://doi.org/10.1139/gen-2013-0069.
13. Tan B, Semple K, Foght J. 2015. Anaerobic alkane biodegradation by cultures enriched from oil sands tailings ponds involves multiple species capable of fumarate addition. FEMS Microbiol Ecol 91:1- 42. https://doi .org/10.1093/femsec/fiv042.
14. Tan B, Fowler SJ, Abu Laban N, Dong X, Sensen CW, Foght J, Gieg LM. 2015. Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples. ISME J 9:2028 -2045. https://doi.org/10.1038/ismej.2015.22.
15. Wawrik B, Mendivelso M, Parisi VA, Suflita JM, Davidova IA, Marks CR, Van Nostrand JD, Liang Y, Zhou J, Huizinga BJ, Stracedil;poć D, Callaghan AV. 2012. Field and laboratory studies on the bioconversion of coal to methane in the San Juan basin. FEMS Microbiol Ecol 81:26-42. http:// femsec.oxfordjournals.org/content/81/1/26.abstract. https://doi.org/10 .1111/j.1574-6941.2011.01272.x.
16. Lyles CN, Le HM, Beasley WH, McInerney MJ, Suflita JM. 2014. Anaerobic hydrocarbon and fatty acid metabolism by syntrophic bacteria and their impact on carbon steel corrosion. Front Microbiol 5:114. http://www .ncbi.nlm.nih.gov/pmc/articles/PMC3978324/. https://doi.org/10.3389/ fmicb.2014.00114.
17. Schink B. 2002. Synergistic interactions in the microbial world. Antonie Leeuwenhoek 81:257-261. https://doi.org/10.1023/A%3A1020579004534.
18. McInerney MJ, Struchtemeyer CG, Sieber J, Mouttaki H, Stams AJM, Schink B, Rohlin L, Gunsalus RP. 2008. Physiology, ecology, phylogeny, and genomics of microorganisms capable of syntrophic metabolism. Ann N Y Acad Sci 1125:58 -72. https://doi.org/10.1196/annals.1419.005.
19. Struchtemeyer CG, Duncan KE, McInerney MJ. 2011. Evidence for syntrophic butyrate metabolism under sulfate-reducing conditions in a hydrocarbon-contaminated aquifer. FEMS Microbiol Ecol 76:289 -300. http://femsec.oxfordjournals.org/content/76/2/289.abstract. https://doi .org/10.1111/j.1574-6941.2011.01046.x.
20. Narihiro T, Nobu MK, Kim NK, Kamagata Y, Liu WT. 2015. The nexus of syntrophy-associated microbiota in anaerobic digestion revealed by long-term enrichment and community survey. Environ Microbiol 17: 1707-1720. https://doi.org/10.1111/1462-2920.12616.
21. Callaghan AV. 2013. Enzymes involved in the anaerobic oxidation of n-alkanes: From methane to long-chain paraffins. Front Microbiol 4:89. https://doi.org/10.3389/fmicb.2013.00089.
22. von Netzer F, Kuntze K, Vogt C, Richnow HH, Boll M, Lueders T. 2016. Functional gene markers for fumarate-adding and dearomatizing key enzymes in anaerobic aromatic hydrocarbon degradation in terrestrial environments. J Mol Microbiol Biotechnol 26:180 -194. http:// www.karger.com/DOI/10.1159/000441946. https://doi.org/10.1159/ 000441946.
23. Ghattas AK, Fischer F, Wick A, Ternes TA. 2017. Anaerobic biodegradation of (emerging) organic contaminants in the aquatic environment. Water Res 116:268 -295. http://www.sciencedirect.com/science/article/ pii/S0043135417300763. https://doi.org/10.1016/j.watres.2017.02.001.
24. Morris JJ, Lenski RE, Zinser ER. 2012. The Black Queen hypothesis: Evolution of dependencies through adaptive gene loss. mBio 3:e00036-12. http:// mbio.asm.org/content/3/2/e00036-12.abstract. https://doi.org/10.1128/ mBio.00036-12.
25. Sieber JR, McInerney MJ, Gunsalus RP. 2012. Genomic insights into syntrophy: The paradigm for anaerobic metabolic cooperation. Annu Rev Microbiol 66:429-452. https://doi.org/10.1146/annurev-micro-090110 -102844.
26. Mee MT, Collins JJ, Church GM, Wang HH. 2014. Syntrophic exchange in synthetic microbial communities. Proc Natl Acad Sci U S A 111: E2149-E2156. https://doi.org/10.1073/pnas.1405641111.
27. Wintermute EH, Silver PA. 2010. Emergent cooperation in microbial metabolism. Mol Syst Biol 6:407. http://msb.embopress.org/content/6/ 1/407.abstract. https://doi.org/10.1038/msb.2010.66.
28. Pande S, Kaftan F, Lang S, Svatoš A, Germerodt S, Kost C. 2016. Privatization of cooperative benefits stabilizes mutualistic cross-feeding interactions in spatially structured environments. ISME J 10:1413-1423. https://doi.org/10.1038/ismej.2015.212.
29. Momeni B, Waite AJ, Shou W. 2013. Spatial self-organization favors heterotypic cooperation over cheating. Elife 2:e00960. https://doi.org/ 10.7554/eLife.00960. https://doi.org/10.7554/eLife.00960.
30. Ponomarova O, Patil KR. 2015. Metabolic interactions in microbial communities: Untangling the Gordian knot. Curr Opin Microbiol 27:37-44. http://www.sciencedirect.com/science/article/pii/S1369527415000788. https:// doi.org/10.1016/j.mib.2015.06.014.
31. Vallenet D, Labarre L, Rouy Z, Barbe V, Bocs S, Cruveiller S, Lajus A, Pascal G, Scarpelli C, Medigue C. 2006. MaGe: A microbial genome annotation system supported by synteny results. Nucleic Acids Res 34:53- 65. http:// www.ncbi.nlm.nih.gov/pmc/articles/PMC1326237/. https://doi.org/10 .1093/nar/gkj406.
32. Wawrik B, Marks CR, Davidova IA, McInerney MJ, Pruitt S, Duncan KE, Suflita JM, Callaghan AV. 2016. Methanogenic paraffin degradation proceeds via alkane addition to fumarate by "Smithella" spp. mediated by a syntrophic coupling with hydrogenotrophic methanogens. Environ Microbiol 18:2604 -2619. https://doi.org/10.1111/1462-2920.13374.
33. Imachi H, Sekiguchi Y, Kamagata Y, Hanada S, Ohashi A, Harada H. 2002. Pelotomaculum thermopropionicum gen. nov., sp. Nov., an anaerobic, thermophilic, syntrophic propionate-oxidizing bacterium. Int J Syst Evol Microbiol 52:1729 -1735. https://doi.org/10.1099/00207713-52-5-1729.
34. Dong X, Droge J, von Toerne C, Marozava S, McHardy AC, Meckenstock RU. 2017. Reconstructing metabolic pathways of a member of the genus Pelotomaculum suggesting its potential to oxidize benzene to carbon dioxide with direct reduction of sulfate. FEMS Microbiol Ecol 93:fiw254. https://doi.org/10.1093/femsec/fiw254.
35. Bak F, Widdel F. 1986. Anaerobic degradation of phenol and phenol derivatives by Desulfobacterium phenolicum sp. Nov. Arch Microbiol 146:177-180. https://doi.org/10.1007/BF00402347.
36. Schnurer A, Schink B, Svensson BH. 1996. Clostridium ultunense sp. Nov., a mesophilic bacterium oxidizing acetate in syntrophic association with a hydrogenotrophic methanogenic bacterium. Int J Syst Bacteriol 46: 1145-1152. https://doi.org/10.1099/00207713-46-4-1145.
37. Fowler SJ, Toth CRA, Gieg LM. 2016. Community structure in methanogenic enrichments provides insight into syntrophic interactions in hydrocarbonimpacted environments. Front Microbiol 7:562. http://www.ncbi.nlm.nih .gov/pmc/articles/PMC4840303/. https://doi.org/10.3389/fmicb.2016.00562.
38. Poulsen M, Schwab C, Jensen BB, Engberg RM, Spang A, Canibe N, Hojberg O, Milinovich G, Fragner L, Schleper C, Weckwerth W, Lund P, Schramm A, Urich T. 2013. Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen. Nat Commun 4:1428. https://doi.org/10.1038/ncomms2432.
39. Pagani I, Lapidus A, Nolan M, Lucas S, Hammon N, Deshpande S, Cheng J-F, Chertkov O, Davenport K, Tapia R, Han C, Goodwin L, Pitluck S, Liolios K, Mavromatis K, Ivanova N, Mikhailova N, Pati A, Chen A, Palaniappan K, Land M, Hauser L, Chang Y-J, Jeffries CD, Detter JC, Brambilla E, Kannan KP, Djao ODN, Rohde M, Pukall R, Spring S, Goker M, Sikorski J, Woyke T, Bristow J, Eisen JA, Markowitz V, Hugenholtz P, Kyrpides NC, Klenk H-P. 2011. Complete genome sequence of Desulfobulbus propionicus type strain (1pr3T). Stand Genomic Sci 4:100 -110. https://doi.org/10.4056/sigs.1613929.
40. Jensen A, Finster K. 2005. Isolation and characterization of Sulfurospirillum carboxydovorans sp. Nov., a new microaerophilic carbon monoxide oxidizing epsilon proteobacterium. Antonie Leeuwenhoek 87:339 -353. https://doi.org/10.1007/s10482-004-6839-y.
41. Gogotova GI, Vainshtein MB. 1989. Description of a sulfate-reducing bacterium, Desulfobacterium macestii sp. Nov., which is capable of autotrophic growth. Microbiology 58:64-68.
42. Stewart EJ. 2012. Growing unculturable bacteria. J Bacteriol 194: 4151-4160. http://jb.asm.org/content/194/16/4151.abstract. https://doi .org/10.1128/JB.00345-12.
43. Banerjee R, Ragsdale SW. 2003. The many faces of vitamin B12: Catalysis by cobalamin-dependent enzymes. Annu Rev Biochem 72:209 -247. https://doi.org/10.1146/annurev.biochem.72.121801.161828.
44. Degnan PH, Barry NA, Mok KC, Taga ME, Goodman AL. 2014. Human gut microbes use multiple transporters to distinguish vitamin B 12 analogs and compete in the gut. Cell Host Microbe 15:47-57. https://doi.org/10 .1016/j.chom.2013.12.007.
45. Zhang Y, Rodionov DA, Gelfand MS, Gladyshev VN. 2009. Comparative genomic analyses of nickel, cobalt and vitamin B12 utilization. BMC Genomics 10:78. https://doi.org/10.1186/1471-2164-10-78.
46. Renz P, Banerjee R. 1999. Biosynthesis of the 5, 6-dimethylbenzimidazole moiety of cobalamin and of the other bases found in natural corrinoids, p 557-575. In Banerjee R (ed), Chemistry and biochemistry of B12. John Wiley & Sons, Inc., New York, NY.
47. Mok KC, Taga ME. 2013. Growth inhibition of Sporomusa ovata by incorporation of benzimidazole bases into cobamides. J Bacteriol 195: 1902-1911. https://doi.org/10.1128/JB.01282-12.
48. Men Y, Seth EC, Yi S, Crofts TS, Allen RH, Taga ME, Alvarez-Cohen L. 2015. Identification of specific corrinoids reveals corrinoid modification in dechlorinating microbial communities. Environ Microbiol 17:4873- 4884. https://doi.org/10.1111/1462-2920.12500.
49. Giovannoni SJ, Thrash JC, Temperton B. 2014. Implications of streamlining theory for microbial ecology. ISME J 8:1553-1565. https://doi.org/10 .1038/ismej.2014.60.
50. Wu X, Holmfeldt K, Hubalek V, Lundin D, Astrom M, Bertilsson S, Dopson M. 2016. Microbial metagenomes from three aquifers in the Fennoscandian shield terrestrial deep biosphere reveal metabolic partitioning among populations. ISME J 10:1192-1203. https://doi.org/10.1038/ismej .2015.185.
51. Heizer EM, Raiford DW, Raymer ML, Doom TE, Miller RV, Krane DE. 2006. Amino acid cost and codon-usage biases in 6 prokaryotic genomes: A whole-genome analysis. Mol Biol Evol 23:1670 -1680. https://doi.org/10 .1093/molbev/msl029.
52. Widdel F, Bak F. 1992. Gram-negative mesophilic sulfate-reducing bacteria, p 3352-3378. In Prokaryotes. Springer, New York, NY.
53. Crocetti G, Murto M, Bjornsson L. 2006. An update and optimisation of oligonucleotide probes targeting methanogenic Archaea for use in fluorescence in situ hybridisation (FISH). J Microbiol Methods 65:194-201. http:// www.sciencedirect.com/science/article/pii/S0167701205002010. https://doi .org/10.1016/j.mimet.2005.07.007.
54. Joshi N, Fass J. 2011. Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files. https://github.com/najoshi/sickle.
55. Brown CT, Howe A, Zhang Q, Pyrkosz AB, Brom TH. 2012. A referencefree algorithm for computational normalization of shotgun sequencing data. arXiv arXiv:1203.4802. https://arxiv.org/abs/1203.4802.
56. Li D, Liu CM, Luo R, Sadakane K, Lam TW. 2015. MEGAHIT: An ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674-1676. http:// bioinformatics.oxfordjournals.org/content/early/2015/01/19/bioinformatics .btv033.abstract. https://doi.org/10.1093/bioinformatics/btv033.
57. Sahlin K, Vezzi F, Nystedt B, Lundeberg J, Arvestad L. 2014. BESST- efficient scaffolding of large fragmented assemblies. BMC Bioinformatics 15:281. http://www.biomedcentral.com/1471-2105/15/281. https://doi .org/10.1186/1471-2105-15-281.
58. Quinlan AR, Hall IM. 2010. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842. http://www.ncbi.nlm.nih .gov/pmc/articles/PMC2832824/. https://doi.org/10.1093/bioinformatics/ btq033.
59. Kang DD, Jeff Froula J, Egan R, Wang Z. 2015. MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities. PeerJ 3:e1165. https://doi.org/10.7717/peerj.1165.
60. Parks DH, Imelfort M, Skennerton CT, Philip Hugenholtz P, Tyson GW. 2015. CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25: 1043-1055. https://doi.org/10.1101/gr.186072.114.
61. Segata N, Bornigen D, Morgan XC, Huttenhower C. 2013. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 4:2304. http://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3760377/. https://doi.org/10.1038/ncomms3304.
62. Seemann T. 2014. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 30:2068-2069. http://bioinformatics.oxfordjournals.org/cgi/content/ long/btu153v1.
63. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer ELL, Tate J, Punta M. 2014. Pfam: The protein families database. Nucleic Acids Res 42: D222-D230. http://nar.oxfordjournals.org/content/42/D1/D222.abstract. https://doi.org/10.1093/nar/gkt1223.
64. Eddy S.R. 2011. Accelerated profile HMM searches. PLoS Comput Biol 7:e1002195. https://doi.org/10.1371/journal.pcbi.1002195.
65. Sinclair L, Osman OA, Bertilsson S, Eiler A. 2015. Microbial community composition and diversity via 16S rRNA gene amplicons: Evaluating the Illumina platform. PLoS One 10:e0116955. https://doi.org/10.1371/ journal.pone.0116955.