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Volume 168, Issue 9

Vitamin B biosynthesis of isolated from the intestinal content of captive common bottlenose dolphins () Free

Abstract

In comparison with terrestrial mammals, dolphins require a large amount of haemoglobin in blood and myoglobin in muscle to prolong their diving time underwater and increase the depth they can dive. The genus is a common gastrointestinal bacterium in dolphins and includes two species: and . Whilst the former produces vitamin B, which is essential for the biosynthesis of haem, a component of haemoglobin and myoglobin, but not produced by mammals, the production ability of the latter remains unknown. The present study aimed to isolate from dolphins and reveal its ability to biosynthesize vitamin B. Three strains of , identified by phylogenetic analyses with 16S rRNA gene and genome-based taxonomy assignment and biochemical features, were isolated from faecal samples collected from two captive common bottlenose dolphins (). A microbioassay using ATCC 7830 showed that the average concentration of vitamin B produced by the three strains was 11 (standard deviation: 2) pg ml. The biosynthesis pathway of vitamin B, in particular, adenosylcobalamin, was detected in the draft genome of the three strains using blastKOALA. This is the first study to isolate from common bottlenose dolphins and reveal its ability of vitamin B biosynthesis, and our findings emphasize the importance of in supplying haemoglobin and myoglobin to dolphins.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Cetobacterium ceti , dolphin , intestinal bacteria and vitamin B12
Funding
This study was supported by the:
  • Japan Society for the Promotion of Science (Award 20J10377)
    • Principle Award Recipient: AkihikoSuzuki
© 2022 The Authors
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2022-09-30
2024-04-25
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References

  1. LeBlanc JG, Milani C, de Giori GS, Sesma F, van Sinderen D et al. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 2013; 24:160–168 [View Article] [PubMed]
     [Google Scholar]
  2. Rucker RB, Zempleni J, Suttie JW, McCormick DB. Handbook of Vitamins, 4th Edn Boca Raton, FL, USA: CRC Press; 2007 [View Article]
     [Google Scholar]
  3. Magnúsdóttir S, Ravcheev D, de Crécy-Lagard V, Thiele I. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front Genet 2015; 6:148 [View Article] [PubMed]
     [Google Scholar]
  4. Martens JH, Barg H, Warren MJ, Jahn D. Microbial production of vitamin B12. Appl Microbiol Biotechnol 2002; 58:275–285 [View Article] [PubMed]
     [Google Scholar]
  5. Bertrand EM, McCrow JP, Moustafa A, Zheng H, McQuaid JB et al. Phytoplankton-bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proc Natl Acad Sci 2015; 112:9938–9943 [View Article]
     [Google Scholar]
  6. Watanabe F, Bito T. Vitamin B12 sources and microbial interaction. Exp Biol Med 2018; 243:148–158 [View Article]
     [Google Scholar]
  7. Ministry of the Environment, Government of Japan Regulation for enforcement of the act on welfare and management of animals; 2006 https://www.env.go.jp/nature/dobutsu/aigo/1_law/files/aigo_kanri_2006_001_en.pdf accessed 2 October 2022
  8. Gimmel AER, Baumgartner K, Liesegang A. Vitamin blood concentration and vitamin supplementation in bottlenose dolphins (Tursiops truncatus) in European facilities. BMC Vet Res 2016; 12:180 [View Article] [PubMed]
     [Google Scholar]
  9. Morris PJ, Johnson WR, Pisani J, Bossart GD, Adams J et al. Isolation of culturable microorganisms from free-ranging bottlenose dolphins (Tursiops truncatus) from the southeastern United States. Vet Microbiol 2011; 148:440–447 [View Article] [PubMed]
     [Google Scholar]
  10. Buck JD, Wells RS, Rhinehart HL, Hansen LJ. Aerobic microorganisms associated with free-ranging bottlenose dolphins in coastal Gulf of Mexico and Atlantic Ocean waters. J Wildl Dis 2006; 42:536–544 [View Article] [PubMed]
     [Google Scholar]
  11. Venn-Watson S, Smith CR, Jensen ED. Primary bacterial pathogens in bottlenose dolphins Tursiops truncatus: needles in haystacks of commensal and environmental microbes. Dis Aquat Organ 2008; 79:87–93 [View Article] [PubMed]
     [Google Scholar]
  12. You L, Ying C, Liu K, Zhang X, Lin D et al. Changes in the fecal microbiome of the Yangtze finless porpoise during a short-term therapeutic treatment. Open Life Sci 2020; 15:296–310 [View Article] [PubMed]
     [Google Scholar]
  13. Wan X, Li J, Cheng Z, Ao M, Tian R et al. The intestinal microbiome of an Indo-Pacific humpback dolphin (Sousa chinensis) stranded near the Pearl River Estuary, China. Integr Zool 2021; 16:287–299 [View Article] [PubMed]
     [Google Scholar]
  14. Tian J, Du J, Lu Z, Han J, Wang Z et al. Distribution of microbiota across different intestinal tract segments of a stranded dwarf minke whale, Balaenoptera acutorostrata. Microbiology Open 2020; 9:10 [View Article]
     [Google Scholar]
  15. Soverini M, Quercia S, Biancani B, Furlati S, Turroni S et al. The bottlenose dolphin (Tursiops truncatus) faecal microbiota. FEMS Microbiol Ecol 2016; 92:fiw055 [View Article] [PubMed]
     [Google Scholar]
  16. Bik EM, Costello EK, Switzer AD, Callahan BJ, Holmes SP et al. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat Commun 2016; 7: [View Article] [PubMed]
     [Google Scholar]
  17. Bai S, Zhang P, Lin M, Lin W, Yang Z et al. Microbial diversity and structure in the gastrointestinal tracts of two stranded short‐finned pilot whales (Globicephala macrorhynchus) and a pygmy sperm whale (Kogia breviceps). Integr Zool 2021; 16:324–335 [View Article]
     [Google Scholar]
  18. Diaz M-A, Bik EM, Carlin KP, Venn‐Watson SK, Jensen ED et al. Identification of Lactobacillus strains with probiotic features from the bottlenose dolphin (Tursiops truncatus). J Appl Microbiol 2013; 115:1037–1051 [View Article]
     [Google Scholar]
  19. Suzuki A, Suzuki M. Antimicrobial activity of Lactococcus lactis subsp. lactis isolated from a stranded Cuvier’s beaked whale (Ziphius cavirostris) against Gram-positive and -negative bacteria. Microorganisms 2021; 9:243 [View Article]
     [Google Scholar]
  20. Danil K, St. Leger J, Dennison S, Bernaldo de Quirós Y, Scadeng M et al. Clostridium perfringens septicemia in a long-beaked common dolphin Delphinus capensis: an etiology of gas bubble accumulation in cetaceans. Dis Aquat Org 2021; 111:183–190 [View Article] [PubMed]
     [Google Scholar]
  21. Jaing C, Thissen JB, Gardner S, McLoughlin K, Slezak T et al. Pathogen surveillance in wild bottlenose dolphins Tursiops truncatus. Dis Aquat Organ 2015; 116:83–91 [View Article] [PubMed]
     [Google Scholar]
  22. Segawa T, Ohno Y, Tsuchida S, Ushida K, Yoshioka M. Helicobacter delphinicola sp. nov., isolated from common bottlenose dolphins Tursiops truncatus with gastric diseases. Dis Aquat Organ 2020; 141:157–169 [View Article] [PubMed]
     [Google Scholar]
  23. Finegold SM, Vaisanen M-L, Molitoris DR, Tomzynski TJ, Song Y et al. Cetobacterium somerae sp. nov. from human feces and emended description of the genus Cetobacterium. Syst Appl Microbiol 2003; 26:177–181 [View Article] [PubMed]
     [Google Scholar]
  24. Foster G, Ross HM, Naylor RD, Collins MD, Ramos CP et al. Cetobacterium ceti gen. nov., sp. nov., a new gram-negative obligate anaerobe from sea mammals. Lett Appl Microbiol 1995; 21:202–206 [View Article]
     [Google Scholar]
  25. Kim DH, Brunt J, Austin B. Microbial diversity of intestinal contents and mucus in rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 2007; 102:1654–1664 [View Article] [PubMed]
     [Google Scholar]
  26. Tsuchiya C, Sakata T, Sugita H. Novel ecological niche of Cetobacterium somerae, an anaerobic bacterium in the intestinal tracts of freshwater fish. Lett Appl Microbiol 2008; 46:43–48 [View Article] [PubMed]
     [Google Scholar]
  27. Roeselers G, Mittge EK, Stephens WZ, Parichy DM, Cavanaugh CM et al. Evidence for a core gut microbiota in the zebrafish. ISME J 2011; 5:1595–1608 [View Article] [PubMed]
     [Google Scholar]
  28. Godoy-Vitorino F, Rodriguez-Hilario A, Alves AL, Gonçalves F, Cabrera-Colon B et al. The microbiome of a striped dolphin (Stenella coeruleoalba) stranded in Portugal. Res Microbiol 2017; 168:85–93 [View Article] [PubMed]
     [Google Scholar]
  29. Robles-Malagamba MJ, Walsh MT, Ahasan MS, Thompson P, Wells RS et al. Characterization of the bacterial microbiome among free-ranging bottlenose dolphins (Tursiops truncatus). Heliyon 2020; 6:e03944 [View Article] [PubMed]
     [Google Scholar]
  30. Suzuki A, Segawa T, Sawa S, Nishitani C, Ueda K et al. Comparison of the gut microbiota of captive common bottlenose dolphins Tursiops truncatus in three aquaria. J Appl Microbiol 2019; 126:31–39 [View Article] [PubMed]
     [Google Scholar]
  31. Suzuki A, Akuzawa K, Kogi K, Ueda K, Suzuki M. Captive environment influences the composition and diversity of fecal microbiota in indo‐pacific bottlenose dolphins, Tursiops aduncus. Mar Mamm Sci 2021; 37:207–219 [View Article]
     [Google Scholar]
  32. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
     [Google Scholar]
  33. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 1994; 22:4673–4680 [View Article] [PubMed]
     [Google Scholar]
  34. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
     [Google Scholar]
  35. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
     [Google Scholar]
  36. Tamura K, Stecher G, Kumar S. MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
     [Google Scholar]
  37. Ryu E. A simple method of differentiation between gram-positive and gram-negative organisms without staining. Kitasato Arch Exp Med 1940; 17:58–63
     [Google Scholar]
  38. Hoff‐Jørgensen E. Microbiological assay of vitamin B12. In Methods of Biochemical Analysis 1954 pp 81–113
     [Google Scholar]
  39. Sato K. Assay methods of vitamin B12. Vitamins 1983; 57:609–616 [View Article]
     [Google Scholar]
  40. Andrews S. FastQC: a quality control tool for high throughput sequence data; 2010 https://www.bioinformatics.babraham.ac.uk/projects/fastqc/
  41. Chen S, Zhou Y, Chen Y, Gu J. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018; 34:884–890 [View Article]
     [Google Scholar]
  42. Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics 2020; 70:e102 [View Article]
     [Google Scholar]
  43. Tanizawa Y, Fujisawa T, Kaminuma E, Nakamura Y, Arita M. DFAST and DAGA: web-based integrated genome annotation tools and resources. Biosci Microbiota Food Health 2016; 35:173–184 [View Article]
     [Google Scholar]
  44. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2018; 30:2068–2069 [View Article] [PubMed]
     [Google Scholar]
  45. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2018; 25:1043–1055 [View Article] [PubMed]
     [Google Scholar]
  46. 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; 50:801–807 [View Article]
     [Google Scholar]
  47. Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol 2022; 428:726–731 [View Article]
     [Google Scholar]
  48. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2018; 68:461–466 [View Article]
     [Google Scholar]
  49. Henson MW, Pitre DM, Weckhorst JL, Lanclos VC, Webber AT et al. Artificial seawater media facilitate cultivating members of the microbial majority from the Gulf of Mexico. mSphere 2022; 1:e00028–00016 [View Article] [PubMed]
     [Google Scholar]
  50. Itoi S, Abe T, Washio S, Ikuno E, Kanomata Y et al. Isolation of halotolerant Lactococcus lactis subsp. lactis from intestinal tract of coastal fish. Int J Food Microbiol 2008; 121:116–121 [View Article]
     [Google Scholar]
  51. Sugita H, Miyajima C, Deguchi Y. The vitamin B12-producing ability of the intestinal microflora of freshwater fish. Aquaculture 1991; 92:267–276 [View Article]
     [Google Scholar]
  52. Warren MJ, Raux E, Schubert HL, Escalante-Semerena JC. The biosynthesis of adenosylcobalamin (vitamin B12). Nat Prod Rep 2002; 19:390–412 [View Article] [PubMed]
     [Google Scholar]
  53. Spencer JB, Stolowich NJ, Roessner CA, Scott AI. The Escherichia coli cysG gene encodes the multifunctional protein, siroheme synthase. FEBS Lett 1993; 335:57–60 [View Article] [PubMed]
     [Google Scholar]
  54. Shelton AN, Seth EC, Mok KC, Han AW, Jackson SN et al. Uneven distribution of cobamide biosynthesis and dependence in bacteria predicted by comparative genomics. ISME J 2019; 13:789–804 [View Article] [PubMed]
     [Google Scholar]
  55. Lu X, Heal KR, Ingalls AE, Doxey AC, Neufeld JD. Metagenomic and chemical characterization of soil cobalamin production. ISME J 2020; 14:53–66 [View Article] [PubMed]
     [Google Scholar]
  56. Hastie GD, Wilson B, Thompson PM. Diving deep in a foraging hotspot: acoustic insights into bottlenose dolphin dive depths and feeding behaviour. Mar Biol 2006; 148:1181–1188 [View Article]
     [Google Scholar]
  57. Ponganis PJ. Diving mammals. Compr Physiol 2011; 1:447–465 [View Article] [PubMed]
     [Google Scholar]
  58. Roth JR, Lawrence JG, Bobik TA. Cobalamin (coenzyme B12): synthesis and biological significance. Annu Rev Microbiol 1996; 50:137–181 [View Article] [PubMed]
     [Google Scholar]
  59. Shoolingin-Jordan PM, Al-Daihan S, Alexeev D, Baxter RL, Bottomley SS et al. 5-Aminolevulinic acid synthase: mechanism, mutations and medicine. Biochim Biophys Acta 2003; 1647:361–366 [View Article] [PubMed]
     [Google Scholar]
  60. Gupta A. Vitamin B12 and folic acid in nutritional anemia in children. Singapore: Springer; 2017 https://doi.org/10.1007/978-981-10-5178-4_8
  61. Kozyraki R, Cases O. Vitamin B12 absorption: mammalian physiology and acquired and inherited disorders. Biochimie 2013; 95:1002–1007 [View Article] [PubMed]
     [Google Scholar]
  62. Seetharam B, Yammani RR. Cobalamin transport proteins and their cell-surface receptors. Expert Rev Mol Med 2003; 5:1–18 [View Article] [PubMed]
     [Google Scholar]
  63. Xiong Y, Brandley MC, Xu S, Zhou K, Yang G. Seven new dolphin mitochondrial genomes and a time-calibrated phylogeny of whales. BMC Evol Biol 2009; 9:20 [View Article] [PubMed]
     [Google Scholar]
  64. Albert MJ, Mathan VI, Baker SJ. Vitamin B12 synthesis by human small intestinal bacteria. Nature 1980; 283:781–782 [View Article] [PubMed]
     [Google Scholar]
  65. Limsuwan T, Lovell RT. Intestinal synthesis and absorption of vitamin B-12 in channel catfish. J Nutr 1981; 111:2125–2132 [View Article] [PubMed]
     [Google Scholar]
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Vitamin B12 biosynthesis of Cetobacterium ceti isolated from the intestinal content of captive common bottlenose dolphins (Tursiops truncatus)
Microbiology 168, 001244 (2022); https://doi.org/10.1099/mic.0.001244
/content/journal/micro/10.1099/mic.0.001244
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