Community structure in methanogenic enrichments provides insight into syntrophic interactions in hydrocarbon-impacted environments

Frontiers in Microbiology

Volumn 7, Issue APR, 2016, Pages

  Fowler, S Jane ^a,b   Toth, Courtney R A ^a   Gieg, Lisa M ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Co occurrence network analysis; Hydrocarbon biodegradation; Methanogenesis; Microbial community composition; Syntrophy

Indexed keywords

ALKANE; ALKYLSUCCINATE SYNTHASE; GLYCOSYLTRANSFERASE; HEXADECANE; HYDROCARBON; METHANE; OCTADECANE; PALMITIC ACID; PETROLEUM; RNA 16S; STEARIC ACID; UNCLASSIFIED DRUG;

ACTINOBACTERIA; ARTICLE; BACTEROIDETES; BIODEGRADATION; BIOME; CHLOROFLEXI; COMMUNITY STRUCTURE; CONTROLLED STUDY; DELTAPROTEOBACTERIA; DNA EXTRACTION; FIRMICUTES; GENE; INOCULATION; METAGENOMICS; METHANOGEN; METHANOGENESIS; MICROBIAL COMMUNITY; MICROBIAL SYNTROPHY; NONHUMAN; ORGANISMAL INTERACTION; POLYMERASE CHAIN REACTION; PYROSEQUENCING; SPIROCHETE;

EID: 84966372826     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00562     Document Type: Article

References (56)

1. Abu Laban, N. A., Dao, A., Semple, K., and Foght, J. (2015). Biodegradation of C7 and C8 iso-alkanes under methanogenic conditions. Environ. Microbiol. 17, 4898-4915. doi: 10.1111/1462-2920.12643
2. Aeckersberg, F., Rainey, F. A., and Widdel, F. (1998). Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch. Microbiol. 170, 361-369. doi: 10.1007/s002030050654
3. An, D., Brown, D., Chatterjee, I., Dong, X., Ramos-Padron, E., Wilson, S. L., et al. (2013). Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond. Genome 56, 612-618. doi: 10.1139/gen-2013-0083
4. Berdugo-Clavijo, C., and Gieg, L. M. (2014). Conversion of crude oil to methane by a microbial consortium enriched from oil reservoir production waters. Front. Microbiol. 5:197. doi: 10.3389/fmicb.2014.00197
5. Berry, D., and Widder, S. (2014). Deciphering microbial interactions and detecting keystone species with co-occurrence networks. Front. Microbiol. 5:219. doi: 10.3389/fmicb.2014.00219
6. Bian, X.-Y., Mbadinga, S. M., Liu, Y.-F., Yang, S.-Z., Liu, J.-F., Ye, R.-Q., et al. (2015). Insights into the anaerobic biodegradation pathway of n-alkanes in oil reservoirs by detection of signature metabolites. Sci. Rep. 5, 9801. doi: 10.1038/srep09801
7. Biddle, A., Stewart, L., Blanchard, J., and Leschine, S. (2013). Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in diverse gut communities. Diversity 5, 627-640. doi: 10.3390/d5030627
8. Callaghan, A. V. (2013). Enzymes involved in the anaerobic oxidation of n-alkanes: from methane to long-chain paraffins. Front. Microbiol. 4:89. doi: 10.3389/fmicb.2013.00089
9. Callaghan, A. V., Davidova, I. A., Savage-Ashlock, K., Parisi, V. A., Gieg, L. M., Suflita, J. M., et al. (2010). Diversity of benzyl- and alkylsuccinate synthase genes in hydrocarbon-impacted environments and enrichment cultures. Environ. Sci. Technol. 44, 7287-7294. doi: 10.1021/es1002023
10. Callaghan, A. V., Wawrik, B., Ní Chadhain, S. M., Young, L. Y., and Zylstra, G. J. (2008). Anaerobic alkane-degrading strain AK-01 contains two alkylsuccinate synthase genes. Biochem. Biophys. Res. Commun. 366, 142-148. doi: 10.1016/j.bbrc.2007.11.094
11. Cheng, L., Ding, C., Li, Q., He, Q., Dai, L. R., and Zhang, H. (2013). DNA-SIP reveals that Syntrophaceae play an important role in methanogenic hexadecane degradation. PLoS ONE 8:e66784. doi: 10.1371/journal.pone.0066784
12. Cravo-Laureau, C., Grossi, V., Raphel, D., Matheron, R., and Hirschlér-Rea, A. (2005). Anaerobic n-alkane metabolism by a sulfate-reducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T. Appl. Environ. Microbiol. 71, 2458-3467
13. Davidova, I. A., Duncan, K. E., Choi, O. K., and Suflita, J. M. (2006). Desulfoglaeba alkanexedens gen. nov., sp. nov., an n-alkane-degrading, sulfate-reducing bacterium. Int. J. Syst. Evol. Microbiol. 56, 2737-2742. doi: 10.1099/ijs.0.64398-0
14. Edwards, E. A., and Grbic-Galic, D. (1994). Anaerobic degradation of toluene and o-xylene by methanogenic consortium. Appl. Environ. Microbiol. 60, 313-322
15. Embree, M., Nagarajan, H., Movahedi, N., Chitsaz, H., and Zengler, K. (2014). Single-cell genome and metatranscriptome sequencing reveal metabolic interactions of an alkane-degrading methanogenic community. ISME J. 8, 757-767. doi: 10.1038/ismej.2013.187
16. Foght, J. (2008). Anaerobic biodegradation of aromatic hydrocarbons: pathways and prospects. J. Mol. Microbiol. Biotechnol. 9, 93-120. doi: 10.1159/000121324
17. Fowler, S. J., Dong, X., Sensen, C. W., Suflita, J. M., and Gieg, L. M. (2012). Methanogenic toluene metabolism: community structure and intermediates. Environ. Microbiol. 14, 754-764. doi: 10.1111/j.1462-2920.2011.02631.x
18. Fowler, S. J., Gutierrez-Zamora, M.-L., Manefield, M., and Gieg, L. M. (2014). Identification of toluene degraders in a methanogenic enrichment culture. FEMS Microbiol. Ecol. 89, 625-636. doi: 10.1111/1574-6941.12364
19. Gieg, L. M., Duncan, K. E., and Suflita, J. M. (2008). Bioenergy production via microbial conversion of residual oil to natural gas. Appl. Environ. Microbiol. 74, 3022-3029. doi: 10.1128/AEM.00119-08
20. Gieg, L. M., Fowler, S. J., and Berdugo-Clavijo, C. (2014). Syntrophic biodegradation of hydrocarbon contaminants. Curr. Opin. Biotechnol. 27, 21-29. doi: 10.1016/j.copbio.2013.09.002
21. Gray, N. D., Sherry, A., Grant, R. J., Rowan, A. K., Hubert, C. R. J., Callbeck, C. M., et al. (2011). The quantitative significance of Syntrophaceae and syntrophic partnerships in methanogenic degradation of crude oil alkanes. Environ. Microbiol. 13, 2957-2975. doi: 10.1111/j.1462-2920.2011.02570.x
22. Gray, N. D., Sherry, A., Hubert, C., Dolfing, J., and Head, I. M. (2010). "Methanogenic degradation of petroleum hydrocarbons in subsurface environments: remediation, heavy oil formation, and energy recovery, " in Advances in Applied Microbiology, eds S. S. Allen, I. Laskin, and M. G. Geoffrey (Cambridge: Academic Press), 137-161
23. Grundmann, O., Behrends, A., Rabus, R., Amann, J., Halder, T., Heider, J., et al. (2008). Genes encoding the candidate enzyme for anaerobic activation of n-alkanes in the denitrifying bacterium HxN1. Environ. Microbiol. 10, 376-385. doi: 10.1111/j.1462-2920.2007.01458.x
24. Heider, J. (2007). Adding handles to unhandy substrates: anaerobic hydrocarbon activation mechanisms. Curr. Opin. Chem. Biol. 11, 188-194. doi: 10.1016/j.cbpa.2007.02.027
25. Jones, D. M., Head, I. M., Gray, N. D., Adams, J. J., Rowan, A. K., Aitken, C. M., et al. (2008). Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451, 176-180. doi: 10.1038/nature06484
26. Kleinsteuber, S., Schleinitzm, K. M., and Vogt, C. (2012). Key players and team play: anaerobic microbial communities in hydrocarbon-contaminated aquifers. Appl. Microbiol. Biotechnol. 94, 851-873. doi: 10.1007/s00253-012-4025-0
27. Liang, B., Wang, L.-Y., Mbadinga, S. M., Liu, J.-F., Yang, S.-Z., Gu, J.-D., et al. (2015). Anaerolineaceae and Methanosaeta turned to be the dominant microorganisms in alkanes-dependent methanogenic culture after long-term of incubation. AMB Express 5, 37. doi: 10.1186/s13568-015-0117-4
28. Mathai, P. P., Zitomer, D. H., and Maki, J. S. (2015). Quantitative detection of syntrophic fatty acid-degrading bacterial communities in methanogenic environments. Microbiology 161, 1189-1197. doi: 10.1099/mic.0.000085
29. Mbadinga, S. M., Li, K.-P., Zhou, L., Wang, L.-Y., Yang, S.-Z., Liu, J.-F., et al. (2012). Analysis of alkane-dependent methanogenic community derived from production water of a high-temperature petroleum reservoir. Appl. Microbiol. Biotechnol. 96, 531-542. doi: 10.1007/s00253-011-3828-8
30. Musat, F. (2015). The anaerobic degradation of gaseous, nonmethane alkanes - From in situ processes to microorganisms. Comput. Struct. Biotechnol. J. 13, 222-228. doi: 10.1016/j.csbj.2015.03.002
31. Nelson, M. C., Morrison, M., and Yu, Z. (2011). A meta-analysis of the microbial diversity observed in anaerobic digesters. Bioresour. Technol. 102, 3730-3739. doi: 10.1016/j.biortech.2010.11.119
32. Notredame, C., Higgins, D. G., and Heringa, J. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217. doi: 10.1006/jmbi.2000.4042
33. Pruesse, E., Quast, C., Knittel, K., Fuchs, B. M., Ludwig, W., Peplies, J., et al. (2007). SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res. 35, 7188-7196. doi: 10.1093/nar/gkm864
34. Rotaru, A. E., Shrestha, P. M., Liu, F., Markovaite, B., Chen, S., Nevin, K. P., et al. (2014). Direct interspecies electron transfer between Geobacter metallireducens and Methanosarcina barkeri. Appl. Environ. Microbiol. 80, 4599-4605. doi: 10.1128/AEM.00895-14
35. Saito, Y., Aoki, M., Hatamoto, M., and Yamaguchi, T. (2015). Presence of a novel methanogenic archaeal lineage in anaerobic digesters inferred from mcrA and 16S rRNA gene phylogenetic analyses. J. Water Environ. Technol. 13, 279-289. doi: 10.2965/jwet.2015.279
36. Savage, K. N., Krumholz, L. R., Gieg, L. M., Parisi, V. A., Suflita, J. M., Allen, J., et al. (2010). Biodegradation of low-molecular-weight alkanes under mesophilic, sulfate-reducing conditions: metabolic intermediates and community patterns. FEMS Microbiol. Ecol. 72, 485-495. doi: 10.1111/j.1574-6941.2010.00866.x
37. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., et al. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504. doi: 10.1101/gr.1239303
38. Sherry, A., Gray, N. D., Ditchfield, A. K., Aitken, C. M., Jones, D. M., Röling, W. F. M., et al. (2013). Anaerobic biodegradation of crude oil under sulphate-reducing conditions leads to only modest enrichment of recognized sulphate-reducing taxa. Int. Biodeter. Biodegr. 81, 105-113. doi: 10.1016/j.ibiod.2012.04.009
39. Sieber, J. R., McInerney, M. J., and Gunsalus, R. P. (2012). Genomic insights into syntrophy: the paradigm for anaerobic metabolic cooperation. Annu. Rev. Microbiol. 66, 429-452. doi: 10.1146/annurev-micro-090110-102844
40. Sikkema, J., De Bont, J. A., and Poolman, B. (1995). Mechanisms of membrane toxicity of hydrocarbons. Microbiol. Rev. 59, 201-222
41. Soh, J., Dong, X., Caffrey, S. M., Voordouw, G., and Sensen, C. W. (2013). Phoenix 2: a locally installable large-scale 16S rRNA gene sequence analysis pipeline with Web interface. J. Biotechnol. 167, 393-403. doi: 10.1016/j.jbiotec.2013.07.004
42. Stadtman, T. C., and Barker, H. A. (1951). Studies on methane fermentation. VIII. Tracer experiments on fatty acid oxidation by methane bacteria. J. Bacteriol. 61, 67-80
43. St-Pierre, B., and Wright, A. D. G. (2013). Comparative metagenomic analysis of bacterial populations in three full-scale mesophilic anaerobic manure digesters. Environ. Biotechnol. 98, 2709-2717. doi: 10.1007/s00253-013-5220-3
44. Symons, G. E., and Buswell, A. M. (1933). The methane fermentation of carbohydrates. J. Am. Chem. Soc. 55, 2028-2036. doi: 10.1021/ja01332a039
45. Tamura, K., and Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512-526
46. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729. doi: 10.1093/molbev/mst197
47. Tan, B., Fowler, S. J., Abu Laban, N., Dong, X., Sensen, C. W., Foght, J., et al. (2015a). Comparative analysis of metagenomes from three methanogenic hydrocarbon-degrading enrichment cultures with 41 environmental samples. ISME J. 9, 2028-2045. doi: 10.1038/ismej.2015.22
48. Tan, B., Nesbø, C., and Foght, J. (2014). Re-analysis of omics data indicates Smithella may degrade alkanes by addition to fumarate under methanogenic conditions. ISME J. 8, 2353-2356. doi: 10.1038/ismej.2014.87
49. Tan, B., Semple, K., and Foght, J. (2015b). Anaerobic alkane biodegradation by cultures enriched from oil sands tailings ponds involves multiple species capable of fumarate addition. FEMS Microbiol. Ecol. 91:fiv042. doi: 10.1093/femsec/fiv042
50. Townsend, G. T., Prince, R. C., and Suflita, J. M. (2003). Anaerobic oxidation of crude oil hydrocarbons by the resident microorganisms of a contaminated anoxic aquifer. Environ. Sci. Technol. 37, 5213-5218. doi: 10.1021/es0264495
51. Vetrovskỳ, T., and Baldrian, P. (2013). The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS ONE 8:e57923. doi: 10.1371/journal.pone.0057923
52. von Netzer, F., Pilloni, G., Kleindienst, S., Krüger, M., Knittel, K., Gründger, F., et al. (2013). Enhanced gene detection assays for fumarate-adding enzymes allow uncovering of anaerobic hydrocarbon degraders in terrestrial and marine systems. Appl. Environ. Microbiol. 79, 543-552. doi: 10.1128/AEM.02362-12
53. Washer, C. E., and Edwards, E. A. (2007). Identification and expression of benzylsuccinate synthase genes in a toluene-degrading methanogenic consortium. Appl. Environ. Microbiol. 73, 1367-1369. doi: 10.1128/AEM.01904-06
54. Widdel, F., and Musat, F. (2010). "Diversity of common principles in enzymatic activation of hydrocarbons, " in Handbook of Hydrocarbon and Lipid Microbiology, ed. K. N. Timmis (Berlin: Springer-Verlag), 983-1009
55. 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 bacterium phylum Chloroflexi. Int. J. Syst. Evol. Microbiol. 56, 1331-1340
56. Zengler, K., Richnow, H., Rosselló-Mora, R., Michaelis, W., and Widdel, F. (1999). Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401, 266-269. doi: 10.1038/45777