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Acetoclastic methanogenesis is likely the dominant biochemical pathway of palmitate degradation in the presence of sulfate

  • Environmental biotechnology
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Abstract

Long chain fatty acids (LCFAs) are important intermediates in the anaerobic degradation of n-alkanes. In order to find out the biochemical processes involved in the degradation of LCFAs, palmitate (a typical LCFA) was used as a substrate, and low-temperature oilfield production fluids were used as a source of microorganisms to establish two anaerobic systems, one with addition of sulfate as exogenous electron acceptor (SP), another without exogenous electron acceptor (MP) and both incubated at room temperature. After more than 2 years of incubation, about 48 and 57.4 % of the palmitate were degraded in samples of MP and SP, respectively. Methane production reached 1408 and 1064 μmol for MP and SP, respectively. Clone libraries of archaeal 16S rRNA genes showed that the predominant archaea in the sulfate-amended cultures (SP) was Methanosaeta whereas Methanocalculus dominated the culture without addition of exogenous sulfate (MP). This observation shows that palmitate could be biodegraded into methane through β-oxidation and acetoclastic methanogenesis in the presence of with or without sulfate. The high occurrence of Methanosaeta in the sulfate-amended system indicates that acetoclastic methanogenesis was not inhibited/little affected by the addition of sulfate. Acetoclastic methanogenesis might be the predominant biochemchimcal pathway of methane generation in enrichment cultures amended with sulfate. These results shed light on alternative methanogenic pathways in the presence of sulfate.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2

  • Amend JP, Shock EL (2001) Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbiol Rev 25:175–243. doi:10.1111/j.1574-6976.2001.tb00576.x

    Article  CAS  PubMed  Google Scholar 

  • Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ (2006) New screening software shows that most recent large 16S rRNA gene clone libraries contain chimeras. Appl Environ Microbiol 72:5734–5741. doi:10.1128/AEM.00556-06

  • Beckmann S, Lueders T, Krüger M, Von Netzer F, Engelen B, Cypionka H (2011) Acetogens and acetoclastic Methanosarcinales govern methane formation in abandoned coal mines. Appl Environ Microbiol 77:3749–3756. doi:10.1128/aem.02818-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Callaghan AV, Gieg LM, Kropp KG, Suflita JM, Young LY (2006) Comparison of mechanisms of alkane metabolism under sulfate-reducing conditions among two bacterial isolates and a bacterial consortium. Appl Environ Microbiol 72:4274–4282. doi:10.1128/aem.02896-05

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Callbeck CM, Agrawal A, Voordouw G (2013) Acetate production from oil under sulfate-reducing conditions in bioreactors injected with sulfate and nitrate. Appl Environ Microbiol 79:5059–5068. doi:10.1128/aem.01251-13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cheng L, Qiu TL, Yin XB, Wu XL, Hu GQ, Deng Y, Zhang H (2007) Methermicoccus shengliensis gen. nov., sp. nov., a thermophilic, methylotrophic methanogen isolated from oil-production water, and proposal of Methermicoccaceae fam. nov. Int J Syst Evol Microbiol 57:2964–2969. doi:10.1099/ijs.0.65049-0

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Shi S, Li Q, Chen J, Zhang H, Lu Y (2014) Progressive degradation of crude oil n-alkanes coupled to methane production under mesophilic and thermophilic conditions. PLoS ONE 9, e113253. doi:10.1371/journal.pone.0113253

    Article  PubMed Central  PubMed  Google Scholar 

  • Colleran E, Finnegan S, Lens P (1995) Anaerobic treatment of sulphate-containing waste streams. Antonie Leeuwenhoek 67:29–46. doi:10.1007/bf00872194

    Article  CAS  PubMed  Google Scholar 

  • Cravo-Laureau C, Grossi V, Raphel D, Matheron R, Hirschler-Réa A (2005) Anaerobic n-alkane metabolism by a sulfate-reducing bacterium, Desulfatibacillum aliphaticivorans Strain CV2803T. Appl Environ Microbiol 71:3458–3467. doi:10.1128/aem.71.7.3458-3467.2005

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dolfing J (2014) Thermodynamic constraints on syntrophic acetate oxidation. Appl Environ Microbiol 80:1539–1541. doi:10.1128/aem.03312-13

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dolfing J, Larter SR, Head IM (2008) Thermodynamic constraints on methanogenic crude oil biodegradation. ISME J 2:442–452. doi:10.1038/ismej.2007.111

    Article  CAS  PubMed  Google Scholar 

  • Dolfing J, Xu A, Gray ND, Larter SR, Head IM (2009) The thermodynamic landscape of methanogenic PAH degradation. Microb Biotechnol 2:566–574. doi:10.1111/j.1751-7915.2009.00096.x

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Embree M, Nagarajan H, Movahedi N, Chitsaz H, 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28:3150–3152. doi:10.1093/bioinformatics/bts565

  • Grabowski A, Blanchet D, Jeanthon C (2005) Characterization of long-chain fatty-acid-degrading syntrophic associations from a biodegraded oil reservoir. Res Microbiol 156:814–821. doi:10.1016/j.resmic.2005.03.009

    Article  CAS  PubMed  Google Scholar 

  • Gray ND, Sherry A, Grant RJ, Rowan AK, Hubert CRJ, Callbeck CM, Aitken CM, Jones DM, Adams JJ, Larter SR, Head IM (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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guan J, Xia LP, Wang LY, Liu JF, Gu JD, Mu BZ (2013) Diversity and distribution of sulfate-reducing bacteria in four petroleum reservoirs detected by using 16S rRNA and dsrAB genes. Int Biodeterior Biodegrad 76:58–66. doi:10.1016/j.ibiod.2012.06.021

    Article  CAS  Google Scholar 

  • Guan J, Zhang BL, Mbadinga S, Liu JF, Gu JD, Mu BZ (2014) Functional genes (dsr) approach reveals similar sulphidogenic prokaryotes diversity but different structure in saline waters from corroding high temperature petroleum reservoirs. Appl Environ Microbiol 98:1871–1882. doi:10.1007/s00253-013-5152-y

    CAS  Google Scholar 

  • Huber T, Faulkner G, Hugenholtz P (2004) Bellerophon: a program to detect chimeric sequences in multiple sequence alignments. Bioinformatics 20:2317–2319. doi:10.1093/bioinformatics/bth226

  • Jones DM, Watson JS, Meredith W, Chen M, Bennett B (2000) Determination of naphthenic acids in crude oils using nonaqueous ion exchange solid-phase extraction. Anal Chem 73:703–707. doi:10.1021/ac000621a

    Article  Google Scholar 

  • Kendall M, Boone D (2006) The Order Methanosarcinales in Dworkin M, Falkow S, Rosenberg E, Schleifer K-H and Stackebrandt E (eds) The Prokaryotes, Springer, New York, pp 244-256. doi: 10.1007/0-387-30743-5_12

  • Kuever J (2014a) The Family Desulfarculaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson EF (eds) The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria. Springer, Berlin, pp 41–44. doi:10.1007/978-3-642-39044-9_270

    Chapter  Google Scholar 

  • Kuever J (2014b) The Family Desulfobacteraceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson EF (eds) The Prokaryotes. Springer, Berlin, pp 45–73. doi:10.1007/978-3-642-39044-9_266

    Chapter  Google Scholar 

  • Kuever J (2014c) The Family Desulfobulbaceae. In: Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson EF (eds) The Prokaryotes: Deltaproteobacteria and Epsilonproteobacteria. Springer, Berlin, pp 75–86. doi:10.1007/978-3-642-39044-9_267

    Chapter  Google Scholar 

  • Lai MC, Chen SC, Shu CM, Chiou MS, Wang CC, Chuang MJ, Hong TY, Liu CC, Lai LJ, Hua JJ (2002) Methanocalculus taiwanensis sp. nov., isolated from an estuarine environment. Int J Syst Evol Microbiol 52:1799–1806. doi:10.1099/ijs.0.01730-0

    Article  CAS  PubMed  Google Scholar 

  • Lee ZM, Bussema C 3rd, Schmidt TM (2009) rrnDB: documenting the number of rRNA and tRNA genes in bacteria and archaea. Nucleic Acids Res 37(database issue):D489–D493. doi:10.1093/nar/gkn689

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics/Comput Appl Biosci 22:1658–1659. doi:10.1093/bioinformatics/btl158

  • Mayumi D, Dolfing J, Sakata S, Maeda H, Miyagawa Y, Ikarashi M, Tamaki H, Takeuchi M, Nakatsu CH, Kamagata Y (2013) Carbon dioxide concentration dictates alternative methanogenic pathways in oil reservoirs. Nat Commun 4.: 1998 doi:10.1038/ncomms2998

  • Mbadinga SM, Wang LY, Zhou L, Liu JF, Gu JD, Mu BZ (2011) Microbial communities involved in anaerobic degradation of alkanes. Int Biodeterior Biodegrad 65:1–13. doi:10.1016/j.ibiod.2010.11.009

    Article  CAS  Google Scholar 

  • Mbadinga S, Li KP, Zhou L, Wang LY, Yang SZ, Liu JF, Gu JD, Mu BZ (2012) Analysis of alkane-dependent methanogenic community derived from production water of a high-temperature petroleum reservoir. Appl Environ Microbiol 96:531–542. doi:10.1007/s00253-011-3828-8

    CAS  Google Scholar 

  • McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:W20–W25. doi:10.1093/nar/gkh435

  • Meredith W, Kelland SJ, Jones DM (2000) Influence of biodegradation on crude oil acidity and carboxylic acid composition. Org Geochem 31:1059–1073. doi:10.1016/S0146-6380(00)00136-4

    Article  CAS  Google Scholar 

  • Noor E, Haraldsdóttir HS, Milo R, Fleming RM (2013) Consistent estimation of Gibbs energy using component contributions. PLoS Comput Biol 9, e1003098. doi:10.1371/journal.pcbi.1003098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pham VD, Hnatow LL, Zhang S, Fallon RD, Jackson SC, Tomb JF, Delong EF, Keeler SJ (2009) Characterizing microbial diversity in production water from an Alaskan mesothermic petroleum reservoir with two independent molecular methods. Environ Microbiol 11:176–187. doi:10.1111/j.1462-2920.2008.01751.x

    Article  CAS  PubMed  Google Scholar 

  • Qu X, Vavilin VA, Mazéas L, Lemunier M, Duquennoi C, He PJ, Bouchez T (2009) Anaerobic biodegradation of cellulosic material: Batch experiments and modelling based on isotopic data and focusing on aceticlastic and non-aceticlastic methanogenesis. Waste Manag 29:1828–1837. doi:10.1016/j.wasman.2008.12.008

    Article  CAS  PubMed  Google Scholar 

  • Rabus R, Hansen T, Widdel F (2013) Dissimilatory sulfate- and sulfur-reducing Prokaryotes. In: Rosenberg E, Delong E, Lory S, Stackebrandt E, Thompson F (eds) The Prokaryotes. Springer, Berlin, pp 309–404. doi:10.1007/978-3-642-30141-4_70

  • Savage KN, Krumholz LR, Gieg LM, Parisi VA, Suflita JM, Allen J, Philp RP, Elshahed MS (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

    Article  CAS  PubMed  Google Scholar 

  • Shimizu S, Upadhye R, Ishijima Y, Naganuma T (2011) Methanosarcina horonobensis sp. nov., a methanogenic archaeon isolated from a deep subsurface miocene formation. Int J Syst Evol Micr 61:2503–2507. doi:10.1099/ijs.0.028548-0

    Article  CAS  Google Scholar 

  • Smith KS, Ingram-Smith C (2007) Methanosaeta, the forgotten methanogen? Trends Microbiol 15:150–155. doi:10.1016/j.tim.2007.02.002

    Article  CAS  PubMed  Google Scholar 

  • Sousa DZ, Pereira MA, Stams AJ, Alves MM, Smidt H (2007) Microbial communities involved in anaerobic degradation of unsaturated or saturated long-chain fatty acids. Appl Environ Microbiol 73:1054–1064. doi:10.1128/AEM.01723-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sousa DZ, Alves JI, Alves MM, Smidt H, Stams AJ (2009) Effect of sulfate on methanogenic communities that degrade unsaturated and saturated long‐chain fatty acids (LCFA). Environ Microbiol 11:68–80. doi:10.1111/j.1462-2920.2008.01740.x

    Article  CAS  PubMed  Google Scholar 

  • Sousa DZ, Balk M, Alves M, Schink B, Mcinerney MJ, Smidt H, Plugge CM, Stams AJM (2010) Degradation of long-chain fatty acids by sulfate-reducing and methanogenic communities. In: Timmis K (ed) Handbook of Hydrocarbon and Lipid Microbiology, 1st edn. Springer, Berlin, pp 963–980. doi:10.1007/978-3-540-77587-4_69

    Chapter  Google Scholar 

  • Tan B, Nesbo C, 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

    Article  PubMed  Google Scholar 

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41(1):100–180

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wang LY, Gao CX, Mbadinga SM, Zhou L, Liu JF, Gu JD, Mu BZ (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. doi:10.1016/j.ibiod.2010.12.010

    Article  CAS  Google Scholar 

  • Yu Y, Lee C, Kim J, Hwang S (2005) Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 89:670–679. doi:10.1002/bit.20347

    Article  CAS  PubMed  Google Scholar 

  • Zellner G, Messner P, Winter J, Stackebrandt E (1998) Methanoculleus palmolei sp. nov., an irregularly coccoid methanogen from an anaerobic digester treating wastewater of a palm oil plant in North-Sumatra, Indonesia. Int J Syst Bacteriol 48:1111–1117. doi:10.1099/00207713-48-4-1111

    Article  CAS  PubMed  Google Scholar 

  • Zhou L, Li KP, Mbadinga S, Yang SZ, Gu JD, Mu BZ (2012) Analyses of n-alkanes degrading community dynamics of a high-temperature methanogenic consortium enriched from production water of a petroleum reservoir by a combination of molecular techniques. Ecotoxicology 21:1680–1691. doi:10.1007/s10646-012-0949-5

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Zheng H, Ai G, Zhang G, Liu D, Liu X, Dong X (2012) The genome characteristics and predicted function of methyl-group oxidation pathway in the obligate aceticlastic methanogens, Methanosaeta spp. PLoS ONE 7, e36756. doi:10.1371/journal.pone.0036756

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (Grant No. 51174092, 41373070, 31200101), the National Natural Science Foundation of China, and the Research Grants Council Joint Research Fund (Grant No. 41161160560).

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The authors declare no competing financial interests.

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Authors and Affiliations

  1. State Key Laboratory of Bioreactor Engineering and Institute of Applied Chemistry, East China University of Science and Technology, Shanghai, 200237, People’s Republic of China

    Lei Lv, Serge Maurice Mbadinga, Li-Ying Wang, Jin-Feng Liu, Bo-Zhong Mu & Shi-Zhong Yang

  2. School of Biological Sciences, The University of Hong Kong, Pokfulam Road, Hong Kong, SAR, People’s Republic of China

    Ji-Dong Gu

  3. Shanghai Collaborative Innovation Center for Biomanufacturing Technology, Shanghai, 200237, People’s Republic of China

    Serge Maurice Mbadinga & Bo-Zhong Mu

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  1. Lei Lv
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  2. Serge Maurice Mbadinga
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  5. Ji-Dong Gu
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Correspondence to Shi-Zhong Yang.

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Lv, L., Mbadinga, S.M., Wang, LY. et al. Acetoclastic methanogenesis is likely the dominant biochemical pathway of palmitate degradation in the presence of sulfate. Appl Microbiol Biotechnol 99, 7757–7769 (2015). https://doi.org/10.1007/s00253-015-6669-z

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