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Description of Gemmobacter aestuarii sp. nov., isolated from estuarine surface water and reclassification of Cereibacter changlensis as Gemmobacter changlensis Chen et al. 2013

  • Asif Hameed
  • Mariyam Shahina
  • Shih-Yao Lin
  • Wen-Ming Chen
  • Yi-Han Hsu
  • Wei-An Lai
  • Chiu-Chung YoungEmail author
Original Paper
  • 18 Downloads

Abstract

A Gram-stain-negative, tyrosine-metabolizing, non-motile, strictly aerobic, non-spore-forming, rod-shaped marine bacterium, designated strain CC-PW-75T, was isolated from the estuarine water off Pintung, Taiwan. Strain CC-PW-75T formed a distinct phyletic lineage associated with Gemmobacter species, sharing the highest 16S rRNA gene sequence similarity with G. megaterium CF17T and G. straminiformis CAM-8T (96.0% each) followed by G. aquatilis IFAM 1031T and G. nectariphilus AST4T (95.8% each). Analysis of the draft genome (3.76 Mbp) revealed the presence of genes encoding light-harvesting complexes, photosynthetic reaction centers and proteins involved in the metabolism of CO, CO2, HCO3 and H2S. However, bacteriochlorophyll a was not detected. Average nucleotide identity values between the genome sequence of CC-PW-75T and the related Gemmobacter species (n = 6) were estimated to be 72.8–76.3%. Polar lipid analysis revealed the presence of phosphatidylglycerol, phosphatidylethanolamine and an unidentified lipid in major amounts, and phosphatidylmonomethylethanolamine, phosphatidylcholine, an unidentified aminolipid and an unidentified lipid in minor amounts. C18:1ω7c and/or C18:1ω6c, C18:0 and C18:1ω7c 11-methyl were identified to be major fatty acids. The DNA G + C content was 66.2 mol% (draft genome sequence). Ubiquinone-10 (Q-10) was the sole respiratory quinone. Based on the polyphasic taxonomic evidence, CC-PW-75T is most likely a novel species of the genus Gemmobacter, affiliated to the family Rhodobacteraceae, for which the name Gemmobacter aestuarii sp. nov. is proposed. The type strain is CC-PW-75T (= JCM 19754T = BCRC 80759T). Also, we propose the reclassification of Cereibacter changlensis as Gemmobacter changlensis Chen et al. 2013 using the polyphasic data presented in this study.

Keywords

Rhodobacteraceae Bacteriochlorophyll RuBisCO Carbon monoxide dehydrogenase Light-harvesting complex 

Notes

Acknowledgements

This work was financially supported by the “Innovation and Development Center of Sustainable Agriculture” from The Featured Areas Research Center Program within the framework of the Higher Education Sprout Project by the Ministry of Education (MOE) (Grant No. 100S0506) in Taiwan.

The GenBank accession number for the 16S rRNA gene sequence of strain CC-PW-75T is KF732818. The draft genome of CC-PW-75T has been deposited at DDBJ/ENA/GenBank under the Accession No. SSND00000000. The version described in this paper is version SSND01000000.

Author contributions

MS isolated the strain and carried out physiological tests and literature survey. SYL identified the strain and performed the fatty acid analysis. WAL conducted the biochemical analysis. AH performed polar lipid, quinone, and other chemotaxonomic analysis. YHH dealt with hydrolysis of macromolecules and physiological tests in part. AH together with WMC and CCY analyzed the raw data and drafted the manuscript.

Compliance with ethical standards

Conflict of interest

Authors declare no existing potential conflict of interest and they were notified about the content of the manuscript.

Human and animal rights statement

No human participants and/or animals were used in this study.

Supplementary material

203_2020_1809_MOESM1_ESM.docx (4.7 mb)
Supplementary file1 (DOCX 4809 kb)

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefGoogle Scholar
  2. Anil Kumar P, Srinivas TNR, Sasikala C, Ramana CV (2007) Rhodobacter changlensis sp. nov., a psychrotolerant, phototrophic, alphaproteobacterium from the Himalayas of India. Int J Syst Evol Microbiol 57:2568–2571CrossRefGoogle Scholar
  3. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M et al (2008) The RAST Server: rapid annotations using subsystems technology. BMC Genomics 9:75CrossRefGoogle Scholar
  4. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477CrossRefGoogle Scholar
  5. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  6. Chen WM, Cho NT, Huang WC, Young CC, Sheu SY (2013) Description of Gemmobacter fontiphilus sp. nov., isolated from a fresh water spring, reclassification of Catellibacterium nectariphilum as Gemmobacter nectariphilus comb. nov., Catellibacterium changlense as Gemmobacter changlensis comb. nov., Catellibacterium aquatile as Gemmobacter aquaticus nom. nov., Catellibacterium caeni as Gemmobacter caeni comb. nov., Catellibacterium nanjingense as Gemmobacter nanjingensis comb. nov., and emended description of the genus Gemmobacter and of Gemmobacter aquatilis. Int J Syst Evol Microbiol 63:470–478CrossRefGoogle Scholar
  7. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, Meyer SD, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466CrossRefGoogle Scholar
  8. Collins MD (1985) Analysis of isoprenoid quinones. Methods Microbiol 18:329–366CrossRefGoogle Scholar
  9. GCG (1995) Wisconsin Package Version 8.1 Program Manual. Computer Group, Madison.Google Scholar
  10. Embley TM, Wait R (1994) Structural lipids of eubacteria. In: Goodfellow M, O'Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley, Chichester, pp 121–161Google Scholar
  11. Euzéby JP (1997) List of bacterial names with standing in nomenclature: a folder available on the internet. Int J Syst Bacteriol 47:590–592CrossRefGoogle Scholar
  12. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefGoogle Scholar
  13. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  14. Fitch WM (1971) Towards defining the course of evolution: minimum change for a specific tree topology. Syst Biol 20:406–416CrossRefGoogle Scholar
  15. Hameed A, Lin SY, Lai WA, Shahina M, Liu YC, Hsu YH et al (2016) Idiomarina tyrosinivorans sp. nov., isolated from estuarine surface water. Int J Syst Evol Microbiol 66:5384–5391CrossRefGoogle Scholar
  16. Heiner CR, Hunkapiller KL, Chen SM, Glass JI, Chen EY (1998) Sequencing multimegabase-template DNA with BigDye terminator chemistry. Genome Res 8:557–561CrossRefGoogle Scholar
  17. Kämpfer P, Kroppenstedt RM (1996) Numerical analysis of fatty acid patterns of coryneform bacteria and related taxa. Can J Microbiol 42:989–1005CrossRefGoogle Scholar
  18. Kämpfer P, Jerzak L, Wilharm G, Golke J, Busse HJ, Glaeser SP (2015) Gemmobacter intermedius sp. nov., isolated from a white stork, (Ciconia ciconia). Int J Syst Evol Microbiol 65:778–783CrossRefGoogle Scholar
  19. Kang JY, Kim MJ, Chun J, Son KP, Jahng KY (2017) Gemmobacter straminiformis sp. nov., isolated from an artificial fountain. Int J Syst Evol Microbiol 67:5019–5025CrossRefGoogle Scholar
  20. Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721CrossRefGoogle Scholar
  21. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  22. Liu JJ, Zhang XQ, Chi FT, Pan J, Sun C, Wu M (2014) Gemmobacter megaterium sp. nov., isolated from coastal planktonic seaweeds. Int J Syst Evol Microbiol 64:66–71CrossRefGoogle Scholar
  23. Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M, Schaal A, Parlett JH (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241CrossRefGoogle Scholar
  24. Murray RGE, Doetsch RN, Robinow CF (1994) Determinative and cytological light microscopy. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society of Microbiology, Washington, pp 21–41Google Scholar
  25. Parte AC (2018) LPSN–list of prokaryotic names with standing in nomenclature (bacterio.net), 20 years on. Int J Syst Evol Microbiol 68:1825–1829CrossRefGoogle Scholar
  26. Rothe B, Fischer A, Hirsch P, Sittig M, Stackebrandt E (1987) The phylogenetic position of the budding bacteria Blastobacter aggregatus and Gemmobacter aquatilis gen., nov. sp. nov. Arch Microbiol 147:92–99CrossRefGoogle Scholar
  27. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  28. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:16Google Scholar
  29. Shahina M, Hameed A, Lin SY, Hsu YH, Liu YC, Cheng IC, Lee MR, Lai WA, Lee RJ, Young CC (2013) Sphingomicrobium astaxanthinifaciens sp. nov., an astaxanthin-producing glycolipid-rich bacterium isolated from surface seawater and emended description of the genus Sphingomicrobium. Int J Syst Evol Microbiol 63:3415–3422CrossRefGoogle Scholar
  30. Sheu SY, Sheu DS, Sheu FS, Chen WM (2013a) Gemmobacter tilapiae sp. nov., a poly-β-hydroxybutyrate-accumulating bacterium isolated from a freshwater pond. Int J Syst Evol Microbiol 63:1550–1556CrossRefGoogle Scholar
  31. Sheu SY, Shiau YW, Wei YT, Chen WM (2013b) Gemmobacter lanyuensis sp. nov., isolated from a freshwater spring. Int J Syst Evol Microbiol 63:4039–4045CrossRefGoogle Scholar
  32. Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, pp 607–654Google Scholar
  33. Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155Google Scholar
  34. Stackebrandt E, Goebel BM (1994) Taxonomic note: a place for DNA–DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. Int J Syst Bacteriol 44:846–849CrossRefGoogle Scholar
  35. Suresh G, Sasikala C, Ramana CV (2015) Reclassification of Gemmobacter changlensis to a new genus as Cereibacter changlensis gen. nov., comb. nov. Int J Syst Evol Microbiol 65:794–798CrossRefGoogle Scholar
  36. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefGoogle Scholar
  37. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  38. Tindall BJ, Rosselló-Móra R, Busse HJ, Ludwig W, Kämpfer P (2010) Notes on the characterization of prokaryote strains for taxonomic purposes. Int J Syst Evol Microbiol 60:249–266CrossRefGoogle Scholar
  39. Watts D, MacBeath JR (2001) Automated fluorescent DNA sequencing on the ABI PRISM 310 Genetic Analyzer. Methods Mol Biol 167:153–170PubMedGoogle Scholar
  40. Yoo Y, Lee DW, Lee H, Kwon BO, Khim JS, Yim UH, Park H, Park B, Choi IG, Kim BS, Jeon SW, Kim GH, Kim JJ (2019) Gemmobacter lutimaris sp nov, a marine bacterium isolated from a tidal flat. Int J Syst Evol Microbiol.  https://doi.org/10.1099/ijsem.0.003375 CrossRefPubMedGoogle Scholar
  41. Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286CrossRefGoogle Scholar
  42. Zheng JW, Chen YG, Zhang J, Ni YY, Li WJ, He J, Li SP (2011) Description of Catellibacterium caeni sp. nov., reclassification of Rhodobacter changlensis Anil Kumar et al. 2007 as Catellibacterium changlense comb. nov. and emended description of the genus Catellibacterium. Int J Syst Evol Microbiol 61:1921–1926CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  1. 1.Department of Soil and Environmental Sciences, College of Agriculture and Natural ResourcesNational Chung Hsing UniversityTaichungTaiwan
  2. 2.Laboratory of Microbiology, Department of Seafood ScienceNational Kaohsiung Marine UniversityKaohsiung CityTaiwan
  3. 3.Innovation and Development Center of Sustainable AgricultureNational Chung Hsing UniversityTaichungTaiwan

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