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Phylogenetic Analysis and Metabolic Potential of Microbial Communities in an Industrial Bagasse Collection Site

  • Environmental Microbiology
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Abstract

Industrial bagasse collection sites at sugar mills are an important resource for biomass-based industries and represent a unique ecological niche in lignocellulose degradation. In this study, microbial community structures at regions with varying microenvironmental conditions contained within a bagasse collection site were explored using tagged 16S rRNA gene pyrosequencing. Overall, remarkable differences in microbial community structures were found in aerobic surface and oxygen-limited interior regions of the pile. A variety of Alphaproteobacteria and Gammaproteobacteria represented the majority of bacteria in the aerobic upper-pile regions with the predominance of acetic acid bacteria towards the outer surface. Diverse Proteobacteria, Bacteroidetes, and Acidobacteria represented the predominant phyla at the exterior soil-contact pile base with an increasing abundance of anaerobic Spirochaetes with the increasing depth, where it shared similar community structures to that in the open-field soil from decomposed bagasse. Using complementary shotgun pyrosequencing, a variety of genes encoding various glycosyl hydrolases targeting cellulose and hemicellulose degradation were identified in the oxygen-limited interior pile base. Most were relevant to orders Clostridiales, Bacteroidales, Sphingobacteriales, and Cytophagales, suggesting their role in lignocellulose degradation in this region, as evidenced by the decrease in cellulose and respective increase in lignin fractions of the biomass. Partial carbon flux in the anoxic region was metabolized through mixed methanogenesis pathways as suggested by the annotated functional genes in methane synthesis. This study gives insights into native microbial community structures and functions in this unique lignocellulose degrading environment and provides the basis for controlling microbial processes important for utilization of bagasse in bio-industries.

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References

  1. Fengel D, Wegener G (1984) Wood: chemistry, ultrastructure, reactions. Walter de Gruyter, Berlin

    Google Scholar 

  2. Kumar R, Singh S, Singh OV (2008) Bioconversion of lignocellulosic biomass: biochemical and molecular perspectives. J Ind Microbiol Biotechnol 35:377–391

    Article  PubMed  CAS  Google Scholar 

  3. Kanokratana P, Uengwetwanit T, Rattanachomsri U, Bunterngsook B, Nimchua T, Tangphatsornruang S, Plengvidhya V, Champreda V, Eurwilaichitr L (2011) Insights into the phylogeny and metabolic potential of a primary tropical peat swamp forest microbial community by metagenomic analysis. Microb Ecol 61:518–528

    Article  PubMed  Google Scholar 

  4. Warnecke F, Luginbuhl P, Ivanova N, Ghassemian M, Richardson TH, Stege JT, Cayouette M, McHardy AC, Djordjevic G, Aboushadi N, Sorek R, Tringe SG, Podar M, Martin HG, Kunin V, Dalevi D, Madejska J, Kirton E, Platt D, Szeto E, Salamov A, Barry K, Mikhailova N, Kyrpides NC, Matson EG, Ottesen EA, Zhang X, Hernandez M, Murillo C, Acosta LG, Rigoutsos I, Tamayo G, Green BD, Chang C, Rubin EM, Mathur EJ, Robertson DE, Hugenholtz P, Leadbetter JR (2007) Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite. Nat 450:560–565

    Article  CAS  Google Scholar 

  5. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125

    Article  PubMed  Google Scholar 

  6. Acosta-Martínez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  Google Scholar 

  7. Humblot C, Guyot JP (2009) Pyrosequencing of tagged 16S rRNA gene amplicons for rapid deciphering of the microbiomes of fermented foods such as pearl millet slurries. Appl Environ Microbiol 75:4354–4361

    Article  PubMed  CAS  Google Scholar 

  8. Callaway TR, Dowd SE, Edrington TS, Anderson RC, Krueger N, Bauer N, Kononoff PJ, Nisbet DJ (2010) Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. J Anim Sci 88:3977–3983

    Article  PubMed  CAS  Google Scholar 

  9. Kiatkittipong W, Wongsuchoto P, Pavasant P (2009) Life cycle assessment of bagasse waste management options. Waste Manag 29:1628–1633

    Article  PubMed  CAS  Google Scholar 

  10. Pandey A, Soccol CR, Nigam P, Soccol VT (2000) Biotechnological potential of agro-industrial residues. I: sugarcane bagasse. Bioresource Technol 74:69–80

    Article  CAS  Google Scholar 

  11. Yadav KR, Chaudhari AB, Sharma RK, Kothari RM (2005) Preservation of bagasse through the application of chemical preservatives. Indian J Chem Technol 12:7–11

    CAS  Google Scholar 

  12. Yadav KR, Patil RP, Chaudhari AB, Sharma RK, Kothari RM (2005) Preservation of bagasse using microbial growth/ enzyme inhibitors as biotech preservatives. Indian J Chem Technol 12:528–533

    CAS  Google Scholar 

  13. Rattanachomsri U, Kanokratana P, Eurwilaichitr L, Igarashi Y, Champreda V (2011) Culture-independent phylogenetic analysis of the microbial community in industrial sugarcane bagasse feedstock piles. Biosci Biotechnol Biochem 75:232–239

    Article  PubMed  CAS  Google Scholar 

  14. Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    PubMed  CAS  Google Scholar 

  15. Kanokratana P, Chanapan S, Pootanakit K, Eurwilaichitr L (2004) Diversity and abundance of bacteria and archaea in the Bor Khlueng hot spring in Thailand. J Basic Microbiol 44:430–444

    Article  PubMed  Google Scholar 

  16. Harnpicharnchai P, Thongaram T, Sriprang R, Champreda V, Tanapongpipat S, Eurwilaichitr L (2007) An efficient purification and fractionation of genomic DNA from soil by modified troughing method. Lett Appl Microbiol 45:387–391

    Article  PubMed  CAS  Google Scholar 

  17. Baker GC, Smith JJ, Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Methods 55:541–555

    Article  PubMed  CAS  Google Scholar 

  18. Meyer M, Stenzel U, Hofreiter M (2008) Parallel tagged sequencing on the 454 platform. Nat Protoc 3:267–278

    Article  PubMed  CAS  Google Scholar 

  19. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinforma 27:2194–2200

    Article  CAS  Google Scholar 

  20. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    Article  PubMed  CAS  Google Scholar 

  21. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  PubMed  CAS  Google Scholar 

  22. Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinforma 18:207–208

    Article  CAS  Google Scholar 

  23. Overbeek R, Begley T, Butler RM, Choudhuri JV, Chuang HY, Cohoon M, de Crecy-Lagard V, Diaz N, Disz T, Edwards R, Fonstein M, Frank ED, Gerdes S, Glass EM, Goesmann A, Hanson A, Iwata-Reuyl D, Jensen R, Jamshidi N, Krause L, Kubal M, Larsen N, Linke B, McHardy AC, Meyer F, Neuweger H, Olsen G, Olson R, Osterman A, Portnoy V, Pusch GD, Rodionov DA, Ruckert C, Steiner J, Stevens R, Thiele I, Vassieva O, Ye Y, Zagnitko O, Vonstein V (2005) The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes. Nucleic Acids Res 33:5691–5702

    Article  PubMed  CAS  Google Scholar 

  24. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinforma 21:3674–3676

    Article  CAS  Google Scholar 

  25. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–238

    Article  PubMed  CAS  Google Scholar 

  26. Edwards RA, Rodriguez-Brito B, Wegley L, Haynes M, Breitbart M, Peterson DM, Saar MO, Alexander S, Alexander EC Jr, Rohwer F (2006) Using pyrosequencing to shed light on deep mine microbial ecology. BMC Genomics 7:57

    Article  PubMed  Google Scholar 

  27. Edward Aul & Associates Inc., E. H. Pechan & Associates Inc. (1993) Emission factor documentation for AP-42 section 1.8 bagasse combustion in sugar mills. http://www.epa.gov/ttnchie1/ap42/ch01/bgdocs/b01s08.pdf. Accessed 23 Jan 2013

  28. Weber S, Stubner S, Conrad R (2001) Bacterial populations colonizing and degrading rice straw in anoxic paddy soil. Appl Environ Microbiol 67:1318–1327

    Article  PubMed  CAS  Google Scholar 

  29. Wang CM, Shyu CL, Ho SP, Chiou SH (2008) Characterization of a novel thermophilic, cellulose-degrading bacterium Paenibacillus sp. strain B39. Lett Appl Microbiol 47:46–53

    Article  PubMed  CAS  Google Scholar 

  30. Doi RH, Kosugi A (2004) Cellulosomes: plant-cell-wall-degrading enzyme complexes. Nat Rev Microbiol 2:541–551

    Article  PubMed  CAS  Google Scholar 

  31. Ohmiya K, Sakka K, Kimura T (2005) Anaerobic bacterial degradation for the effective utilization of biomass. Biotechnol Bioproc E 10:482–493

    Article  CAS  Google Scholar 

  32. Xu Q, Bayer EA, Goldman M, Kenig R, Shoham Y, Lamed R (2004) Architecture of the Bacteroides cellulosolvens cellulosome: description of a cell surface-anchoring scaffoldin and a family 48 cellulase. J Bacteriol 186:968–977

    Article  PubMed  CAS  Google Scholar 

  33. Ward NL, Challacombe JF, Janssen PH, Henrissat B, Coutinho PM, Wu M, Xie G, Haft DH, Sait M, Badger J, Barabote RD, Bradley B, Brettin TS, Brinkac LM, Bruce D, Creasy T, Daugherty SC, Davidsen TM, DeBoy RT, Detter JC, Dodson RJ, Durkin AS, Ganapathy A, Gwinn-Giglio M, Han CS, Khouri H, Kiss H, Kothari SP, Madupu R, Nelson KE, Nelson WC, Paulsen I, Penn K, Ren Q, Rosovitz MJ, Selengut JD, Shrivastava S, Sullivan SA, Tapia R, Thompson LS, Watkins KL, Yang Q, Yu C, Zafar N, Zhou L, Kuske CR (2009) Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol 75:2046–2056

    Article  PubMed  CAS  Google Scholar 

  34. Ransom-Jones E, Jones DL, McCarthy AJ, McDonald JE (2012) The Fibrobacteres: an important phylum of cellulose-degrading bacteria. Microb Ecol 63:267–281

    Article  PubMed  CAS  Google Scholar 

  35. Yan ZC, Wang B, Li YZ, Gong X, Zhang HQ, Gao PJ (2003) Morphologies and phylogenetic classification of cellulolytic myxobacteria. Syst Appl Microbiol 26:104–109

    Article  PubMed  Google Scholar 

  36. Zhang H, Hutcheson SW (2011) Complex expression of the cellulolytic transcriptome of Saccharophagus degradans. Appl Environ Microbiol 77:5591–5596

    Article  PubMed  CAS  Google Scholar 

  37. Garcia JL, Patel BK, Ollivier B (2000) Taxonomic, phylogenetic, and ecological diversity of methanogenic Archaea. Anaerobe 6:205–226

    Article  PubMed  CAS  Google Scholar 

  38. Raspor P, Goranovic D (2008) Biotechnological applications of acetic acid bacteria. Crit Rev Biotechnol 28:101–124

    Article  PubMed  CAS  Google Scholar 

  39. Allgaier M, Reddy A, Park JI, Ivanova N, D’haeseleer P, Lowry S, Sapra R, Hazen TC, Simmons BA, VanderGheynst JS, Hugenhotz P (2010) Targeted discovery of glycoside hydrolases from a switchgrass-adapted compost community. PLoS One 5:e8812

    Article  PubMed  Google Scholar 

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Acknowledgments

This project was supported by a research grant from the National Center for Genetic Engineering and Biotechnology, National Science and Technology Development Agency (P-10-10848). Kanokratana P. was supported by the Royal Golden Jubilee Scholarship (PHD/0260/2549). Manuscript proofreading by Dr. Philip Shaw is appreciated.

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Authors and Affiliations

  1. Enzyme Technology Laboratory, Bioresources Technology Unit, National Center for Genetic Engineering and Biotechnology (BIOTEC), 113 Thailand Science Park, Paholyothin Road, Klong Luang, Pathumthani, 12120, Thailand

    Pattanop Kanokratana, Wuttichai Mhuantong, Thanaporn Laothanachareon, Lily Eurwilaichitr & Verawat Champreda

  2. Genome Institute, National Center for Genetic Engineering and Biotechnology, Thailand Science Park, Klong Luang, Pathumthani, 12120, Thailand

    Sithichoke Tangphatsornruang

  3. Institute of Molecular Biosciences, Mahidol University, Salaya, Nakornpathom, 73170, Thailand

    Pattanop Kanokratana & Kusol Pootanakit

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  1. Pattanop Kanokratana
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  2. Wuttichai Mhuantong
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Correspondence to Kusol Pootanakit or Verawat Champreda.

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Kanokratana, P., Mhuantong, W., Laothanachareon, T. et al. Phylogenetic Analysis and Metabolic Potential of Microbial Communities in an Industrial Bagasse Collection Site. Microb Ecol 66, 322–334 (2013). https://doi.org/10.1007/s00248-013-0209-0

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  • DOI: https://doi.org/10.1007/s00248-013-0209-0

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