1887

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY logo

Volume 73, Issue 3

, gen. nov., sp. nov., a novel succinic acid producing bacterium isolated from a steer on a high grain diet Open Access

Abstract

This study presents MP1D12 (=NRRL B-67553=NCTC 14480), an isolate from the ruminal content of an Angus steer fed a high grain diet. Phenotypic and genotypic traits of the isolate were explored. MP1D12 was found to be a strictly anaerobic, catalase-negative, oxidase-negative, coccoid bacterium that frequently grows in chains. Analysis of metabolic products as a result of carbohydrate fermentation showed succinic acid as the major organic acid produced with lactic acid and acetic acid as minor products. Phylogenetic analysis of MP1D12 based on 16S rRNA nucleotide sequence and amino acid sequences from the whole genome presents a divergent lineage from other members in the family . 16S rRNA sequence comparison, whole genome average nucleotide identity digital DNA–DNA hybridization and average amino acid identity results suggest that MP1D12 represents a novel species in a novel genus within the family . We propose the creation of the genus in which MP1D12 represents the type strain for the novel species .

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Chordicoccus , genome and rumen
© 2023 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.

Erratum

An erratum has been published for this content:
Corrigendum: , gen. nov., sp. nov., a novel succinic acid producing bacterium isolated from a steer on a high grain diet
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.005751
2023-03-01
2024-05-11
Loading full text...

Full text loading...

/deliver/fulltext/ijsem/73/3/ijsem005751.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.005751&mimeType=html&fmt=ahah

References

  1. Stackebrandt E. The family Lachnospiraceae. In Rosenberg E, DeLong EF, Stackebrandt E, Lory S, Thompson F. eds The Prokaryotes, 4th edn. Berlin: Springer-Verlag; 2014 pp 197–201
     [Google Scholar]
  2. Meehan CJ, Beiko RG. A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 2014; 6:703–713 [View Article]
     [Google Scholar]
  3. Stackebrandt E, Kramer I, Swiderski J, Hippe H. Phylogenetic basis for a taxonomic dissection of the genus Clostridium. FEMS Immunol Med Microbiol 1999; 24:253–258 [View Article]
     [Google Scholar]
  4. Ludwig W, Schleifer KH, Whitman WB et al. Revised road map to the phylum Firmicutes. In DeVos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. eds Bergey’s Manual of Systematic Bacteriology: Volume 3 the Firmicutes, 2nd edn. New York: Springer New York; 2009 pp 1–13
     [Google Scholar]
  5. Rosero JA, Killer J, Sechovcová H, Mrázek J, Benada O et al. Reclassification of Eubacterium rectale (Hauduroy et al. 1937) Prévot 1938 in a new genus Agathobacter gen. nov. as Agathobacter rectalis comb. nov., and description of Agathobacter ruminis sp. nov., isolated from the rumen contents of sheep and cows. Int J Syst Evol Microbiol 2016; 66:768–773 [View Article]
     [Google Scholar]
  6. Yutin N, Galperin MY. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ Microbiol 2013; 15:2631–2641 [View Article]
     [Google Scholar]
  7. Sakamoto M, Iino T, Ohkuma M. Faecalimonas umbilicata gen. nov., sp. nov., isolated from human faeces, and reclassification of Eubacterium contortum, Eubacterium fissicatena and Clostridium oroticum as Faecalicatena contorta gen. nov., comb. nov., Faecalicatena fissicatena comb. nov. and Faecalicatena orotica comb. nov. Int J Syst Evol Microbiol 2017; 67:1219–1227 [View Article]
     [Google Scholar]
  8. Shetty SA, Zuffa S, Bui TPN, Aalvink S, Smidt H et al. Reclassification of Eubacterium hallii as Anaerobutyricum hallii gen. nov., comb. nov., and description of Anaerobutyricum soehngenii sp. nov., a butyrate and propionate-producing bacterium from infant faeces. Int J Syst Evol Microbiol 2018; 68:3741–3746 [View Article]
     [Google Scholar]
  9. Cai S, Dong X. Cellulosilyticum ruminicola gen. nov., sp. nov., isolated from the rumen of yak, and reclassification of Clostridium lentocellum as Cellulosilyticum lentocellum comb. nov. Int J Syst Evol Microbiol 2010; 60:845–849 [View Article]
     [Google Scholar]
  10. Allen-Vercoe E, Daigneault M, White A, Panaccione R, Duncan SH et al. Anaerostipes hadrus comb. nov., a dominant species within the human colonic microbiota; reclassification of eubacterium hadrum moore et al. Anaerobe 1976; 18(5):523–529
     [Google Scholar]
  11. Seshadri R, Leahy SC, Attwood GT, Teh KH, Lambie SC et al. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. Nat Biotechnol 2018; 36:359–367 [View Article] [PubMed]
     [Google Scholar]
  12. Tap J, Mondot S, Levenez F, Pelletier E, Caron C et al. Towards the human intestinal microbiota phylogenetic core. Environ Microbiol 2009; 11:2574–2584 [View Article]
     [Google Scholar]
  13. Kittelmann S, Seedorf H, Walters WA, Clemente JC, Knight R et al. Simultaneous amplicon sequencing to explore co-occurrence patterns of bacterial, archaeal and eukaryotic microorganisms in rumen microbial communities. PLoS One 2013; 8:e47879 [View Article]
     [Google Scholar]
  14. Gosalbes MJ, Durbán A, Pignatelli M, Abellan JJ, Jiménez-Hernández N et al. Metatranscriptomic approach to analyze the functional human gut microbiota. PLoS One 2011; 6:e17447 [View Article]
     [Google Scholar]
  15. Henderson G, Cox F, Ganesh S, Jonker A, Young W et al. Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range. Sci Rep 2015; 5:14567 [View Article]
     [Google Scholar]
  16. Creevey CJ, Kelly WJ, Henderson G, Leahy SC. Determining the culturability of the rumen bacterial microbiome. Microb Biotechnol 2014; 7:467–479 [View Article]
     [Google Scholar]
  17. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006; 444:1027–1031 [View Article]
     [Google Scholar]
  18. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes 2008; 32:1720–1724 [View Article]
     [Google Scholar]
  19. Frank DN, St Amand AL, Feldman RA, Boedeker EC, Harpaz N et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A 2007; 104:13780–13785 [View Article]
     [Google Scholar]
  20. Li F, Guan LL. Metatranscriptomic profiling reveals linkages between the active rumen microbiome and feed efficiency in beef cattle. Appl Environ Microbiol 2017; 83:e00061-17 [View Article]
     [Google Scholar]
  21. Thoetkiattikul H, Mhuantong W, Laothanachareon T, Tangphatsornruang S, Pattarajinda V et al. Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing. Curr Microbiol 2013; 67:130–137 [View Article]
     [Google Scholar]
  22. Tong J, Zhang H, Yang D, Zhang Y, Xiong B et al. Illumina sequencing analysis of the ruminal microbiota in high-yield and low-yield lactating dairy cows. PLoS One 2018; 13:e0198225 [View Article]
     [Google Scholar]
  23. Yang B, Le J, Wu P, Liu J, Guan LL et al. Alfalfa intervention alters rumen microbial community development in Hu lambs during early life. Front Microbiol 2018; 9:574 [View Article]
     [Google Scholar]
  24. Dehority BA. Pectin-fermenting bacteria isolated from the bovine rumen. J Bacteriol 1969; 99:189–196 [View Article]
     [Google Scholar]
  25. Biddle A, Stewart L, Blanchard J, Leschine S. Untangling the genetic basis of fibrolytic specialization by Lachnospiraceae and Ruminococcaceae in Diverse Gut communities. Diversity 2013; 5:627–640 [View Article]
     [Google Scholar]
  26. Duncan SH, Barcenilla A, Stewart CS, Pryde SE, Flint HJ. Acetate utilization and butyryl coenzyme A (CoA):acetate-CoA transferase in butyrate-producing bacteria from the human large intestine. Appl Environ Microbiol 2002; 68:5186–5190 [View Article]
     [Google Scholar]
  27. Rainey FA, Family V et al. Lachnospiraceae fam. nov. In DeVos P, Garrity GM, Jones D, Krieg NR, Ludwig W et al. eds Bergey’s Manual of Systematic Bacteriology: Volume Three the Firmicutes New York:Springer-Verlag: 2009 pp 921–968
     [Google Scholar]
  28. Gagen EJ, Padmanabha J, Denman SE, McSweeney CS. Hydrogenotrophic culture enrichment reveals rumen lachnospiraceae and ruminococcaceae acetogens and hydrogen-responsive bacteroidetes from pasture-fed cattle. FEMS Microbiol Lett 2015:362 [View Article]
     [Google Scholar]
  29. Zhang XM, Medrano RF, Wang M, Beauchemin KA, Ma ZY et al. Corn oil supplementation enhances hydrogen use for biohydrogenation, inhibits methanogenesis, and alters fermentation pathways and the microbial community in the rumen of goats. J Anim Sci 2019; 97:4999–5008 [View Article]
     [Google Scholar]
  30. Grubb JA, Dehority BA. Variation in colony counts of total viable anaerobic rumen bacteria as influenced by media and cultural methods. Appl Environ Microbiol 1976; 31:262–267 [View Article]
     [Google Scholar]
  31. Bartholomew JW, Mittwer T. The Gram stain. Bacteriol Rev 1952; 16:1–29 [View Article]
     [Google Scholar]
  32. Jain M, Koren S, Miga KH, Quick J, Rand AC et al. Nanopore sequencing and assembly of a human genome with ultra-long reads. Nat Biotechnol 2018; 36:338–345 [View Article]
     [Google Scholar]
  33. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article]
     [Google Scholar]
  34. Heuer H, Krsek M, Baker P, Smalla K, Wellington EM. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microbiol 1997; 63:3233–3241 [View Article]
     [Google Scholar]
  35. Wylensek D, Hitch TCA, Riedel T, Afrizal A, Kumar N et al. A collection of bacterial isolates from the pig intestine reveals functional and taxonomic diversity. Nat Commun 2020; 11:6389 [View Article]
     [Google Scholar]
  36. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
     [Google Scholar]
  37. Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM et al. Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 2014; 42:D633–42 [View Article]
     [Google Scholar]
  38. Wade WG. Eubacterium. In Whitman WB, Rainey F, Kämpfer P, Trujillo ME, DeVos P. eds Bergey’s Manual of Systematics of Archaea and Bacteria: Volume 3 the Firmicutes, 2nd edn. New York: Wiley; 2015 pp 1–36
     [Google Scholar]
  39. Mukherjee A, Lordan C, Ross RP, Cotter PD. Gut microbes from the phylogenetically diverse genus Eubacterium and their various contributions to gut health. Gut Microbes 2020; 12:1802866 [View Article]
     [Google Scholar]
  40. Wiegel J, Tanner R, Rainey FA et al. An introduction to the family clostridiaceae. Prokaryotes 2006; 4:654–678
     [Google Scholar]
  41. Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun 2013; 4:2304 [View Article]
     [Google Scholar]
  42. Chaumeil P-A, Mussig AJ, Hugenholtz P, Parks DH. GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 2019; 36:1925–1927 [View Article]
     [Google Scholar]
  43. Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil P-A et al. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res 2022; 50:D785–D794 [View Article] [PubMed]
     [Google Scholar]
  44. Parks DH, Rinke C, Chuvochina M, Chaumeil P-A, Woodcroft BJ et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol 2017; 2:1533–1542 [View Article] [PubMed]
     [Google Scholar]
  45. Marçais G, Delcher AL, Phillippy AM, Coston R, Salzberg SL et al. MUMmer4: a fast and versatile genome alignment system. PLoS Comput Biol 2018; 14:e1005944 [View Article]
     [Google Scholar]
  46. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: architecture and applications. BMC Bioinformatics 2009; 10:421 [View Article]
     [Google Scholar]
  47. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
     [Google Scholar]
  48. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and archaea based on A standard genome relatedness index. MBio 2020
     [Google Scholar]
  49. Barco RA, Garrity GM, Scott JJ, Amend JP, Nealson KH et al. A genus definition for bacteria and archaea based on genome relatedness and taxonomic affiliation. bioRxiv 2018
     [Google Scholar]
  50. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
     [Google Scholar]
  51. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: A database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
     [Google Scholar]
  52. Meier-Kolthoff JP, Klenk H-P, Göker M. Taxonomic use of DNA G+C content and DNA-DNA hybridization in the genomic age. Int J Syst Evol Microbiol 2014; 64:352–356 [View Article] [PubMed]
     [Google Scholar]
  53. Rodriguez-R LM, Konstantinidis KT. Bypassing cultivation to identify bacterial species. Microbe Magazine 2014; 9:111–118 [View Article]
     [Google Scholar]
  54. 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]
     [Google Scholar]
  55. Wirth JS, Whitman WB. Phylogenomic analyses of a clade within the roseobacter group suggest taxonomic reassignments of species of the genera Aestuariivita, Citreicella, Loktanella, Nautella, Pelagibaca, Ruegeria, Thalassobius, Thiobacimonas and Tropicibacter, and the proposal of six novel genera. Int J Syst Evol Microbiol 2018; 68:2393–2411 [View Article]
     [Google Scholar]
  56. 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]
     [Google Scholar]
  57. Luo C, Rodriguez-R LM, Konstantinidis KT. MyTaxa: an advanced taxonomic classifier for genomic and metagenomic sequences. Nucleic Acids Res 2014; 42:e73 [View Article]
     [Google Scholar]
  58. Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol 2005; 187:6258–6264 [View Article]
     [Google Scholar]
  59. Brenner DJ, Staley JT, Krieg NR. Classification of procaryotic organisms and the concept of bacterial speciation. In Whitman WB, Rainey F, Kämpfer P, Trujillo ME, Chun J et al. eds Bergey’s Manual of Systematics of Archaea and Bacteria, 2nd edn. New York: Springer-Verlag; 2015 pp 1–9
     [Google Scholar]
  60. Avgustin G, Wallace RJ, Flint HJ. Phenotypic diversity among ruminal isolates of Prevotella ruminicola: proposal of Prevotella brevis sp. nov., Prevotella bryantii sp. nov., and Prevotella albensis sp. nov. and redefinition of Prevotella ruminicola. Int J Syst Bacteriol 1997; 47:284–288 [View Article]
     [Google Scholar]
  61. Whitman WB, Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME et al. Bergey’s Manual of Systematic Bacteriology, 2nd edn. New York: Springer-Verlag; 2012
     [Google Scholar]
  62. Cotta M, Forster R. The family Lachnospiraceae, including the genera Butyrivibrio, Lachnospira and Roseburia. In Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E. eds The Prokaryotes vol 4 pp 1002–1021
     [Google Scholar]
  63. Van Gylswyk NO, Van Der Toorn JJTK. Description and designation of a neotype strain of Eubacterium cellulosolvens (Cillobacterium cellulosolvens bryant, small, bouma and robinson) holdeman and moore. Int J Bacteriol 1986; 36:275–277 [View Article]
     [Google Scholar]
  64. Whitford MF, Yanke LJ, Forster RJ, Teather RM. Lachnobacterium bovis gen. nov., sp. nov., a novel bacterium isolated from the rumen and faeces of cattle. Int J Syst Evol Microbiol 2001; 51:1977–1981 [View Article]
     [Google Scholar]
  65. Downes J, Munson MA, Radford DR, Spratt DA, Wade WG. Shuttleworthia satelles gen. nov., sp. nov., isolated from the human oral cavity. Int J Syst Evol Microbiol 2002; 52:1469–1475 [View Article]
     [Google Scholar]
  66. Moon CD, Pacheco DM, Kelly WJ, Leahy SC, Li D et al. Reclassification of Clostridium proteoclasticum as Butyrivibrio proteoclasticus comb. nov., a butyrate-producing ruminal bacterium. Int J Syst Evol Microbiol 2008; 58:2041–2045 [View Article]
     [Google Scholar]
  67. Kopečný J, Zorec M, Mrázek J, Kobayashi Y, Marinšek-Logar R. Butyrivibrio hungatei sp. nov. and Pseudobutyrivibrio xylanivorans sp. nov.,butyrate-producing bacteria from the rumen. Int J Syst Evol Microbiol 2003; 53(1):201–209
     [Google Scholar]
  68. Willems A, Collins MD. Butyrivibrio. In Whitman WB, Rainey F, Kämpfer P, Trujillo ME, Chun J et al. eds Bergey’s Manual of Systematics of Archaea and Bacteria: Volume 3 the Firmicutes, 2nd edn. New York: Wiley; 2015 pp 1–20
     [Google Scholar]
  69. Bryant MP, Small N. The anarobic monotrihous butrichous butric acid-producing curved ROD-shaped bacteria of the rumen. J Bacteriol 1956; 72:16–21 [View Article]
     [Google Scholar]
  70. Van Gylswyk NO, Hippe H, Rainey FA. Pseudobutyrivibrio ruminis gen. nov., sp. nov., a butyrate-producing bacterium from the rumen that closely resembles Butyrivibrio fibrisolvens in phenotype. Int J Syst Evol Microbiol 1996; 46(2):559–563
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/ijsem/10.1099/ijsem.0.005751
Loading
Chordicoccus furentiruminis, gen. nov., sp. nov., a novel succinic acid producing bacterium isolated from a steer on a high grain diet
Int J Syst Evol Microbiol 73, 005751 (2023); https://doi.org/10.1099/ijsem.0.005751
/content/journal/ijsem/10.1099/ijsem.0.005751
/content/journal/ijsem/10.1099/ijsem.0.005751
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

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