1887

Abstract

Strain MDTJ8 is a chain-elongating thermophilic bacterium isolated from a thermophilic acidogenic anaerobic digestor treating human waste while producing the high commodity chemical -caproate. The strain grows and produces formate, acetate, -butyrate, -caproate and lactate from mono-, di- and polymeric saccharides at 37–60 °C (optimum, 50–55 °C) and at pH 5.0–7.0 (optimum, pH 6.5). The organism is an obligate anaerobe, is motile and its cells form rods (0.3–0.5×1.0–3.0 µm) that stain Gram-positive and occur primarily as chains. Phylogenetic analysis of both the 16S rRNA gene and full genome sequence shows that strain MDTJ8 belongs to a group that consists of mesophylic chain-elongating bacteria within the family , being nearest to EA1 (94.8 %) and BS-1 (93.7 %). Its genome (1.96 Mbp) with a G+C content of 49.6 mol% is remarkably smaller than those of other chain-elongating bacteria of the family . Pairwise average nucleotide identity and DNA–DNA hybridization values between strain MDJT8 and its mesophilic family members are less than 70 and 35 %, respectively, while pairwise average amino acid identity values are less than 68 %. In addition, strain MDJT8 uses far less carbohydrate and non-carbohydrate substrates compared to its nearest family members. The predominant cellular fatty acids of strain MDTJ8 are C, C DMA (dimethyl acetal) and C, while its polar lipid profile shows three unidentified glycophospholipids, 11 glycolipids, 13 phospholipids and six unidentified lipids. No respiratory quinones and polyamines are detected. Based on its phylogenetic, genotypic, morphological, physiological, biochemical and chemotaxonomic characteristics, strain MDTJ8 represents a novel species and novel genus of the family and gen. nov., sp. nov. is proposed as its name. The type strain is MDTJ8 (=DSM 114174=LMG 32615=NCCB 100883).

Funding
This study was supported by the:
  • MELiSSA Foundation (Award 4000114262/15/NL/JC)
    • Principle Award Recipient: TinhVan Nguyen
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005893
2023-05-18
2024-05-18
Loading full text...

Full text loading...

References

  1. Carvajal-Arroyo JM, Andersen SJ, Ganigué R, Rozendal RA, Angenent LT et al. Production and extraction of medium chain carboxylic acids at a semi-pilot scale. J Chem Eng 2021; 416:127886 [View Article]
    [Google Scholar]
  2. De Groof V, Coma M, Arnot T, Leak DJ, Lanham AB. Medium chain carboxylic acids from complex organic feedstocks by mixed culture fermentation. Molecules 2019; 24:1–32 [View Article] [PubMed]
    [Google Scholar]
  3. Seedorf H, Fricke WF, Veith B, Brüggemann H, Liesegang H et al. The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci U S A 2008; 105:2128–2133 [View Article] [PubMed]
    [Google Scholar]
  4. Van Nguyen T, Viver T, Mortier J, Liu B, Smets I et al. Isolation and characterization of a thermophilic chain elongating bacterium that produces the high commodity chemical N-caproate from polymeric carbohydrates. Bioresour Technol 2023; 367:128170 [View Article] [PubMed]
    [Google Scholar]
  5. Moset V, Poulsen M, Wahid R, Højberg O, Møller HB. Mesophilic versus thermophilic anaerobic digestion of cattle manure: methane productivity and microbial ecology. Microb Biotechnol 2015; 8:787–800 [View Article] [PubMed]
    [Google Scholar]
  6. Fernández-Rodríguez J, Pérez M, Romero LI. Comparison of mesophilic and thermophilic dry anaerobic digestion of OFMSW: Kinetic analysis. Chem Eng J 2013; 232:59–64 [View Article]
    [Google Scholar]
  7. Suhartini S, Heaven S, Banks CJ. Comparison of mesophilic and thermophilic anaerobic digestion of sugar beet pulp: performance, dewaterability and foam control. Bioresour Technol 2014; 152:202–211 [View Article] [PubMed]
    [Google Scholar]
  8. Hendrickx L, De Wever H, Hermans V, Mastroleo F, Morin N et al. Microbial ecology of the closed artificial ecosystem MELiSSA (Micro-Ecological Life Support System Alternative): reinventing and compartmentalizing the Earth’s food and oxygen regeneration system for long-haul space exploration missions. Res Microbiol 2006; 157:77–86 [View Article] [PubMed]
    [Google Scholar]
  9. Kim B-C, Seung Jeon B, Kim S, Kim H, Um Y et al. Caproiciproducens galactitolivorans gen. nov., sp. nov., a bacterium capable of producing caproic acid from galactitol, isolated from a wastewater treatment plant. Int J Syst Evol Microbiol 2015; 65:4902–4908 [View Article] [PubMed]
    [Google Scholar]
  10. Flaiz M, Baur T, Brahner S, Poehlein A, Daniel R et al. Caproicibacter fermentans gen. nov., sp. nov., a new caproate-producing bacterium and emended description of the genus Caproiciproducens. Int J Syst Evol Microbiol 2020; 70:4269–4279 [View Article] [PubMed]
    [Google Scholar]
  11. Gu Y, Zhu X, Lin F, Shen C, Li Y et al. Caproicibacterium amylolyticum gen. nov., sp. nov., a novel member of the family Oscillospiraceae isolated from pit clay used for making Chinese strong aroma-type liquor. Int J Syst Evol Microbiol 2021; 71: [View Article] [PubMed]
    [Google Scholar]
  12. Ludwig W, Strunk O, Westram R, Richter L, Meier H et al. ARB: A software environment for sequence data. Nucleic Acids Res 2004; 32:1363–1371 [View Article] [PubMed]
    [Google Scholar]
  13. Ludwig W, Viver T, Westram R, Francisco Gago J, Bustos-Caparros E et al. Release LTP_12_2020, featuring a new ARB alignment and improved 16S rRNA tree for prokaryotic type strains. Syst Appl Microbiol 2021; 44:126218 [View Article] [PubMed]
    [Google Scholar]
  14. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W et al. SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007; 35:7188–7196 [View Article] [PubMed]
    [Google Scholar]
  15. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 2006; 22:2688–2690 [View Article] [PubMed]
    [Google Scholar]
  16. Wang H, Gu Y, Zhao D, Qiao Z, Zheng J et al. Caproicibacterium lactatifermentans sp. nov., isolated from pit clay used for the production of Chinese strong aroma-type liquor. Int J Syst Evol Microbiol 2022; 72:1–9 [View Article] [PubMed]
    [Google Scholar]
  17. Kim M, Oh HS, Park SC, Chun J. Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 2014; 64:346–351 [View Article] [PubMed]
    [Google Scholar]
  18. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  20. Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ Preprints 2016 [View Article]
    [Google Scholar]
  21. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article] [PubMed]
    [Google Scholar]
  22. Lanave C, Preparata G, Saccone C, Serio G. A new method for calculating evolutionary substitution rates. J Mol Evol 1984; 20:86–93 [View Article] [PubMed]
    [Google Scholar]
  23. Sabath N, Ferrada E, Barve A, Wagner A. Growth temperature and genome size in bacteria are negatively correlated, suggesting genomic streamlining during thermal adaptation. Genome Biol Evol 2013; 5:966–977 [View Article] [PubMed]
    [Google Scholar]
  24. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J. JSpeciesWS: A web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 2016; 32:929–931 [View Article] [PubMed]
    [Google Scholar]
  25. Meier-Kolthoff JP, Göker M. TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 2019; 10:2182 [View Article] [PubMed]
    [Google Scholar]
  26. Konstantinidis KT, Tiedje JM. Genomic insights that advance the species definition for prokaryotes. Proc Natl Acad Sci U S A 2005; 102:2567–2572 [View Article] [PubMed]
    [Google Scholar]
  27. Goris J, Konstantinidis KT, Klappenbach JA, Coenye T, Vandamme P et al. DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. Int J Syst Evol Microbiol 2007; 57:81–91 [View Article] [PubMed]
    [Google Scholar]
  28. Qin Q-L, Xie B-B, Zhang X-Y, Chen X-L, Zhou B-C et al. A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 2014; 196:2210–2215 [View Article] [PubMed]
    [Google Scholar]
  29. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
    [Google Scholar]
  30. Nicholson AC, Gulvik CA, Whitney AM, Humrighouse BW, Bell ME et al. Division of the genus chryseobacterium: observation of discontinuities in amino acid identity values, a possible consequence of major extinction events, guides transfer of nine species to the genus epilithonimonas, eleven species to the genus kaistella, a. Int J Syst Evol Microbiol 2020; 70:4432–4450
    [Google Scholar]
  31. Park M-J, Kim YJ, Park M, Yu J, Namirimu T et al. Establishment of genome based criteria for classification of the family Desulfovibrionaceae and proposal of two novel genera, Alkalidesulfovibrio gen. nov. and Salidesulfovibrio gen. nov. Front Microbiol 2022; 13:738205 [View Article] [PubMed]
    [Google Scholar]
  32. Liu A, Zhang Y-J, Cheng P, Peng Y-J, Blom J et al. Whole genome analysis calls for a taxonomic rearrangement of the genus Colwellia. Antonie van Leeuwenhoek 2020; 113:919–931 [View Article] [PubMed]
    [Google Scholar]
  33. Esquivel-Elizondo S, Bağcı C, Temovska M, Jeon BS, Bessarab I et al. The isolate Caproiciproducens sp. 7D4C2 produces n-caproate at mildly acidic conditions from Hexoses: genome and rBOX comparison with related strains and chain-elongating bacteria. Front Microbiol 2020; 11:594524 [View Article] [PubMed]
    [Google Scholar]
  34. Leber AL. Clinical Microbiology Procedures Handbook, 4th edn. Washington, DC, USA: ASM Press; 2016 [View Article]
    [Google Scholar]
  35. Brewer JH. Clear liquid mediums for the ‘Aerobic’ cultivation of anaerobes. JAMA 1940; 115:598 [View Article]
    [Google Scholar]
  36. Hirsch A, Grinsted E. Methods for the growth and enumeration of anaerobic spore-formers from cheese, with observations on the effect of nisin. J Dairy Res 1954; 21:101–110 [View Article]
    [Google Scholar]
  37. Holdeman LV, Cato EP, Moore WE. Anaerobic Laboratory Manual, 4th edn. Blacksburg: Virginia Polytechnic Institute and State University; 1977
    [Google Scholar]
  38. Mező E, Hartmann-Balogh F, Madarászné Horváth I, Bufa A, Marosvölgyi T et al. Effect of culture conditions on fatty acid profiles of bacteria and lipopolysaccharides of the genus Pseudomonas-GC-MS analysis on ionic liquid-based column. Molecules 2022; 27:1–21 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005893
Loading
/content/journal/ijsem/10.1099/ijsem.0.005893
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error