Advertisement

Metagenomic analysis and characterization of acidogenic microbiome and effect of pH on organic acid production

  • Nasir Ali
  • Hui Gong
  • Abdulmoseen Segun Giwa
  • Quan Yuan
  • Kaijun WangEmail author
Original Paper

Abstract

Organic acid production including lactate and acetate is an economically attractive technology that has gained momentum worldwide over the past years. These series of action need to be performed by an esoteric and complex microbial community, in which different members have distinct roles in the establishment of a collective organization. In this study, we analyzed the bioma from bioreactors with various pH conditions of 4.0, 5.0 and 6.0 (R1, R2 and R3), respectively, involved in acidogenic digestion for stable production of various organic acids by means of high-throughput Illumina sequencing, disclosing thousands of genes and extracting more than 53 microbial genomes. At pH 5.0, the hydrolysis reaction was enhanced and thus the lactic acid fermentation was stably improved to 45.96 mm/L and acetic acid to 73.77 mm/L. R2 was found with the most suitable pH condition for stable organic acids production as Lactobacilli and Bifidobacteria were the major members. Both the members have the key roles in heterofermentation and produce higher transcripts of key encoding enzymes involved in the dominant heterofermentation pathways.

Keywords

CSTR Acidogenic fermentation Metagenomics Microbial community structure KEGG analysis 

Notes

Acknowledgements

This work was supported by Major Science and Technology Program for Water Pollution Control and Treatment of China (Grant No. 2017ZX07102-004), and National Natural Science Foundation of China (Grant No. 21206084). We are grateful to University of Chinese Academy of Sciences, China for additional support.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest. All the authors read and approved the final manuscript.

Supplementary material

203_2019_1676_MOESM1_ESM.docx (276 kb)
Supplementary material 1 (DOCX 276 kb)

References

  1. Agler MAM, Spirito CM, Usack JG, Werner JJ, Angenent LT (2002) Chain elongation with reactor microbiomes: upgrading dilute ethanol to medium chain carboxylates. Energy Environ Sci 5:8189–8192CrossRefGoogle Scholar
  2. APHA (1998) Standard methods for the examination of water and wastewater, 20th ed. Washington DCGoogle Scholar
  3. Axelsson L, Holck A, Birkeland SE, Aukrust T, Blom H (1993) Cloning and nucleotide-sequence of a gene from Lactobacillus sake lb706 necessary for sakacin-a production and immunity. Appl Environ Microbiol 59:2868–2875Google Scholar
  4. Chang HN, Kim N, Kang J, Jeong C (2010) Biomass-derived volatile fatty acid platform for fuels and chemicals. Biotechnol Bioprocess Eng 15:1–10CrossRefGoogle Scholar
  5. Chen YG, Jiang S, Yuan HY, Zhou Q, Gu GW (2007) Hydrolysis and acidification of waste activated sludge at different pHs. Water Resour 41:683–689Google Scholar
  6. Cogan TM, Jordan KM (1994) Metabolism of Leuconostoc bacteria. Dairy Sci 77:2704–2717CrossRefGoogle Scholar
  7. De Francisci D, Kougias PG, Treu L, Campanaro S, Angelidaki I (2015) Microbial diversity and dynamicity of biogas reactors due to radical changes of feedstock composition. Biores Technol 176:56–64CrossRefGoogle Scholar
  8. Eikmeyer FG, Rademacher A, Hanreich A, Hennig M, Jaenicke S, Maus I, Wibberg D, Zakrzewski M, Puhler A, Klocke M (2013) Detailed analysis of metagenome datasets obtained from biogas-producing microbial communities residing in biogas reactors does not indicate the presence of putative pathogenic microorganisms. Biotechnol Biofuels 6:49CrossRefGoogle Scholar
  9. Holzapfel WH, Wood BJB (2014) Lactic acid bacteria biodiversity and taxonomy, 1st edn. Wiley-Blackwell press, New YorkCrossRefGoogle Scholar
  10. Howe AC, Jansson JK, Malfatti SA, Tringe SG, Tiedje JM, Brown CT (2014) Tackling soil diversity with the assembly of large, complex metagenomes. Proc Natl Acad Sci 111:4904–4909CrossRefGoogle Scholar
  11. Itoh Y, Tada K, Kanno T, Horiuchi JI (2012) Selective production of lactic acid in continuous anaerobic acidogenesis by extremely low pH operation. Biosci Bioeng 114:537–539CrossRefGoogle Scholar
  12. Jiang Y, Marang L, Kleerebezem R, Muyzer G, van Loosdrecht MCM (2011) Polyhydroxybutyrate production from lactate using a mixed microbial culture. Biotechnol Bioeng 108:2022–2035CrossRefGoogle Scholar
  13. Kandler O (1983) Carbohydrate metabolism in lactic acid bacteria. Antonie van leeuwenhoek J Microbiol 49:209–244CrossRefGoogle Scholar
  14. Kim M, Gomec CY, Ahn Y, Speece RE (2003) Hydrolysis and acidogenesis of particulate organic material in mesophilic and thermophilic anaerobic digestion. Environ Technol 24:1183–1190CrossRefGoogle Scholar
  15. Kougias PG, De Francisci D, Treu L, Campanaro S, Angelidaki I (2014) Microbial analysis in biogas reactors suffering by foaming incidents. Biores Technol 167:24–32CrossRefGoogle Scholar
  16. Krause L, Diaz NN, Edwards RA, Gartemann KH, Kromeke H, Neuweger H, Puhler A, Runte KJ, Schluter A, Stoye J (2008) Taxonomic composition and gene content of a methane-producing microbial community isolated from a biogas reactor. Biotechnology 136:91–101Google Scholar
  17. Krober M, Bekel T, Diaz NN, Goesmann A, Jaenicke S, Krause L, Miller D, Runte KJ, Viehover P, Puhler A (2009) Phylogenetic characterization of a biogas plant microbial community integrating clone library 16S-rDNA sequences and metagenome sequence data obtained by 454-pyrosequencing. Biotechnology 142:38–49Google Scholar
  18. Langille MG, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Thurber RLV, Knight R (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821CrossRefGoogle Scholar
  19. Li A, Chu Y, Wang X, Ren L, Yu J, Liu X (2013) A pyrosequencing-based metagenomic study of methane-producing microbial community in solid-state biogas reactor. Biotechnol Biofuels 6:3CrossRefGoogle Scholar
  20. Maus JE, Ingham SC (2003) Employment of stressful conditions during culture production to enhance subsequent cold- and acid-tolerance of bifidobacteria. Appl Microbiol 95:146–154CrossRefGoogle Scholar
  21. Mazzoli R, Bosco F, Mizrahi I, Bayer EA, Pessione E (2014) Towards lactic acid bacteria-based biorefineries. Biotechnol Adv 32:1216–1236CrossRefGoogle Scholar
  22. Mingxia Z, Lance CS, Giovana T, Wan-Ting C, Yan Z, Ken N, Wanyi Q, Yuanhui Z, Kaijun W (2017) Anaerobic digestion of wastewater generated from the hydrothermal liquefaction of Spirulina: toxicity assessment and minimization. Energy Convers Manage 141:420–428CrossRefGoogle Scholar
  23. Ragsdale SW, Pierce E (2008) Acetogenesis and the Wood-Ljungdahl pathway of CO2 fixation. Biochimica Et Biophysica Acta-Proteins Proteom 1784:1873–1898CrossRefGoogle Scholar
  24. Rasic JK, Kurmann JK (1983) Bifidobacteria and their role. Microbiological, nutritional-physiological, medical and technological aspects and bibliography. Exp Suppl 39:1–295Google Scholar
  25. Reis MAM, Serafim LS, Lemos PC, Ramos AM, Aguiar FR, Van Loosdrecht MCM (2003) Production of polyhydroxyalkanoates by mixed microbial cultures. Bioprocess Biosystem Eng 25:377–385CrossRefGoogle Scholar
  26. Riviere D, Desvignes V, Pelletier E, Chaussonnerie S, Guermazi S, Weissenbach J, Li T, Camacho P, Sghir A (2009) Towards the definition of a core of microorganisms involved in anaerobic digestion of sludge. ISME 3:700–714CrossRefGoogle Scholar
  27. Sandoval LCJ, Vergara MM, De Carreno AM, Castillo MEF (2009) Microbiological characterization and specific methanogenic activity of anaerobe sludges used in urban solid waste treatment. Waste Manage 29:704–711CrossRefGoogle Scholar
  28. Schluter A, Bekel T, Diaz NN, Dondrup M, Eichenlaub R, Gartemann KH, Krahn I, Krause L, Kromeke H, Kruse O (2008) The metagenome of a biogas producing microbial community of a production-scale biogas plant fermenter analysed by the 454-pyrosequencing technology. Biotechnology 136:77–90Google Scholar
  29. Steinbusch KJJ (2000) Liquid biofuel production from volatile fatty acids. PhD. Thesis, Wageningen University, WageningenGoogle Scholar
  30. Takahashi N (2003) Acid-neutralizing activity during amino acid fermentation by Porphyromonas gingivalis, Prevotella intermedia and Fusobacterium nucleatum. Oral Microbial Immunol 18:109–113CrossRefGoogle Scholar
  31. Temudo MF, Kleerbezem R, van Loosdrecht M (2007) Influence of the pH on (open) mixed culture fermentation of glucose: a chemostat study. Biotechnol Bioeng 98:69–79CrossRefGoogle Scholar
  32. Thiago OB, Fernand SG, Mario LL, Henrique VA, Gillian E, Luiz CB (2014) Homo- and heterofermentative lactobacilli differently affect sugarcane-based fuel ethanol fermentation. Antonie Van Leeuwenhoek 105:169–177CrossRefGoogle Scholar
  33. Traversi D, Villa S, Lorenzi E, Degan R, Gilli G (2012) Application of a real-time qPCR method to measure the methanogen concentration during anaerobic digestion as an indicator of biogas production capacity. Environ Manag 111:173–177Google Scholar
  34. Vanwonterghem I, Jensen PD, Dennis PG, Hugenholtz P, Rabaey K, Tyson GW (2015) Deterministic processes guide long-term synchronised population dynamics in replicate anaerobic digesters. ISME 8:2015–2028CrossRefGoogle Scholar
  35. Wang K, Yin J, Shen DS, Li N (2014) Anaerobic digestion of food waste for volatile fatty acids (VFAs) production with different types of inoculum: effect of pH. Bioresour Technol 161:395–401CrossRefGoogle Scholar
  36. Wirth R, Kovacs E, Maroti G, Bagi Z, Rakhely G, Kovacs KL (2012) Characterization of a biogas-producing microbial community by short-read next generation DNA sequencing. Biotechnol Biofuels 5:41CrossRefGoogle Scholar
  37. Wommack KE, Bhavsar J, Ravel J (2008) Metagenomics: read length matters. Appl Environ Microbiol 74:1453–1463CrossRefGoogle Scholar
  38. Yang Y, Yu K, Xia Y, Lau FTK, Tang DTW, Fung WC (2014) Metagenomic analysis of sludge from full-scale anaerobic digesters operated in municipal wastewater treatment plants. Appl Microbiol Biotechnol 98:5709–5718CrossRefGoogle Scholar
  39. Yu HQ, Fang HHP (2002) Acidogenesis of dairy wastewater at various pH levels. Water Sci Technol 45:201–206CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nasir Ali
    • 1
    • 2
  • Hui Gong
    • 1
  • Abdulmoseen Segun Giwa
    • 1
  • Quan Yuan
    • 1
  • Kaijun Wang
    • 1
    Email author
  1. 1.State Key Joint Laboratory of Environment Simulation and Pollution Control, School of EnvironmentTsinghua UniversityBeijingChina
  2. 2.Qingdao Institute of Bioenergy and Bioprocess TechnologyUniversity of Chinese Academy of SciencesQingdaoPeople’s Republic of China

Personalised recommendations