Ulvibacterium marinum gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae, isolated from a culture of the green alga Ulva prolifera

Abstract

A Gram-stain negative, aerobic, rod-shaped, and non-motile bacterium, designated strain CCMM003T, was isolated from a culture of the green alga Ulva prolifera. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain CCMM003T belongs to the family Flavobacteriaceae and exhibits a close relationship to Pseudozobellia thermophila DSM 19858T (92.5%). Optimal growth occurred in the presence of 4% (w/v) NaCl, at pH 7.0 and 30 °C. The polar lipids of strain CCMM003T consisted of phosphatidylethanolamine and six unidentified lipids. The predominant isoprenoid quinone was MK-6. The major fatty acids were iso-C15:0, iso-C15:1 G, iso-C17:0 3-OH and summed feature 3 (C16:1ω7c and/or iso-C15:0 2-OH). The DNA G + C content of strain CCMM003T calculated on the basis of the genome sequence was 41.2 mol% and the genome size was 5.9 Mbp. On the basis of data from this polyphasic study, strain CCMM003T is considered to represent a novel genus and species of the family Flavobacteriaceae, for which the name Ulvibacterium marinum gen. nov., sp. nov. is proposed. The type strain is CCMM003T (= MCCC 1K03244T =KCTC 52639T).

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References

  1. Bae SS, Kwon KK, Yang SH, Lee H-S, Kim S-J, Lee J-H (2007) Flagellimonas eckloniae gen. nov., sp. nov., a mesophilic marine bacterium of the family Flavobacteriaceae, isolated from the rhizosphere of Ecklonia kurome. Int J Syst Evol Microbiol 57:1050–1054. https://doi.org/10.1099/ijs.0.64565-0

    Article  CAS  PubMed  Google Scholar 

  2. Barbeyron T, L’Haridon S, Corre E, Kloareg B, Potin P (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51:985–997. https://doi.org/10.1099/00207713-51-3-985

    Article  CAS  PubMed  Google Scholar 

  3. Bernardet J-F (2015) Flavobacteriaceae. In: Whitman WB et al (eds) Bergey’s manual of systematics of archaea and bacteria. Wiley, Chichester. https://doi.org/10.1002/9781118960608.fbm00069

    Google Scholar 

  4. Bernardet J-F, Segers P, Vancanneyt M, Berthe F, Kersters K, Vandamme P (1996) Cutting a gordian knot: emended classification and description of the genus Flavobacterium, emended description of the family Flavobacteriaceae, and proposal of Flavobacterium hydatis nom. nov. (Basonym, Cytophaga aquatilis Strohl and Tait 1978). Int J Syst Bacteriol 46:128–148

    Article  Google Scholar 

  5. Bernardet J-F, Nakagawa Y, Holmes B (2002) Proposed minimal standards for describing new taxa of the family Flavobacteriaceae and emended description of the family. Int J Syst Evol Microbiol 52:1049–1070. https://doi.org/10.1099/ijs.0.02136-0

    CAS  Article  Google Scholar 

  6. Beveridge TJ, Lawrence JR, Murray RG (2007) Sampling and staining for light microscopy. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM, Snyder LR (eds) Methods for general and molecular microbiology. American Society of Microbiology, Washington, DC, pp 19–33

    Google Scholar 

  7. Collins MD (1994) Isoprenoid quinones. In: Goodfellow M, O’Donnell AG (eds) Chemical methods in prokaryotic systematics. Wiley, Chichester, pp 265–309

    Google Scholar 

  8. Fukui Y, Abe M, Kobayashi M, Saito H, Oikawa H, Yano Y, Satomi M (2012) Polaribacter porphyrae sp. nov., isolated from the red alga Porphyra yezoensis, and emended descriptions of the genus Polaribacter and two Polaribacter species. Int J Syst Evol Microbiol 63:1665–1672. https://doi.org/10.1099/ijs.0.041434-0

    Article  CAS  PubMed  Google Scholar 

  9. Jooste PJ (1985) The taxonomy and significance of Flavobacterium-Cytophaga strains from dairy sources. University of Orange Free State, Bloemfontein

    Google Scholar 

  10. Kim J-Y, Oh D-C (2012) Winogradskyella jejuensis sp. nov., a marine bacterium isolated from a brown alga Carpopeltis affinis. J Microbiol 50:888–892. https://doi.org/10.1007/s12275-012-2447-0

    Article  CAS  PubMed  Google Scholar 

  11. Kim J-Y, Park S-H, Seo G-Y, Kim Y-J, Oh D-C (2015) Winogradskyella eckloniae sp. nov., a marine bacterium isolated from the brown alga Ecklonia cava. Int J Syst Evol Microbiol 65:2791–2796. https://doi.org/10.1099/ijs.0.000334

    Article  CAS  PubMed  Google Scholar 

  12. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  Google Scholar 

  13. Kwon KK, Lee YK, Lee HK (2006) Costertonia aggregata gen. nov., sp. nov., a mesophilic marine bacterium of the family Flavobacteriaceae, isolated from a mature biofilm. Int J Syst Evol Microbiol 56:1349–1353. https://doi.org/10.1099/ijs.0.64168-0

    Article  CAS  PubMed  Google Scholar 

  14. Kwon YM et al (2018) Euzebyella algicola sp. nov., a marine bacterium of the family Flavobacteriaceae, isolated from green algae. Int J Syst Evol Microbiol 68:764–768. https://doi.org/10.1099/ijsem.0.002581

    Article  CAS  PubMed  Google Scholar 

  15. Lee H-S, Kwon KK, Yang S-H, Bae SS, Park CH, Kim S-J, Lee J-H (2008) Description of Croceitalea gen. nov. in the family Flavobacteriaceae with two species, Croceitalea eckloniae sp. nov. and Croceitalea dokdonensis sp. nov., isolated from the rhizosphere of the marine alga Ecklonia kurome. Int J Syst Evol Microbiol 58:2505–2510. https://doi.org/10.1099/ijs.0.65697-0

    Article  CAS  PubMed  Google Scholar 

  16. Lemos ML, Toranzo AE, Barja JL (1985) Modified medium for the oxidation-fermentation test in the identification of marine bacteria. Appl Environ Microb 49:1541–1543

    CAS  Google Scholar 

  17. Lin B, Lu G, Zheng Y, Xie W, Li S, Hu Z (2011) Aquimarina agarilytica sp. nov., an agarolytic species isolated from a red alga. Int J Syst Evol Microbiol 62:869–873. https://doi.org/10.1099/ijs.0.027136-0

    Article  CAS  PubMed  Google Scholar 

  18. Lucena T et al (2010) Euzebyella saccharophila gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae. Int J Syst Evol Microbiol 60:2871–2876. https://doi.org/10.1099/ijs.0.020875-0

    Article  CAS  PubMed  Google Scholar 

  19. Lyman J, Fleming RH (1940) Composition of sea water J Mar Res 3:134–146

    CAS  Google Scholar 

  20. 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 2:233–241

    Article  CAS  Google Scholar 

  21. Nedashkovskaya OI et al (2003) Mesonia algae gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi (Kutz) Kornm. Int J Syst Evol Microbiol 53:1967–1971. https://doi.org/10.1099/ijs.0.02626-0

    Article  CAS  PubMed  Google Scholar 

  22. Nedashkovskaya OI, Kim SB, Han SK, Lysenko AM, Mikhailov VV, Bae KS (2004a) Arenibacter certesii sp. nov., a novel marine bacterium isolated from the green alga Ulva fenestrata. Int J Syst Evol Microbiol 54:1173–1176. https://doi.org/10.1099/ijs.0.02872-0

    Article  CAS  PubMed  Google Scholar 

  23. Nedashkovskaya OI et al (2004b) Ulvibacter litoralis gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from the green alga Ulva fenestrata. Int J Syst Evol Microbiol 54:119–123. https://doi.org/10.1099/ijs.0.02757-0

    Article  CAS  PubMed  Google Scholar 

  24. Nedashkovskaya OI, Kim SB, Lee KH, Bae KS, Frolova GM, Mikhailov VV, Kim IS (2005) Pibocella ponti gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae isolated from the green alga Acrosiphonia sonderi. Int J Syst Evol Microbiol 55:177–181. https://doi.org/10.1099/ijs.0.63251-0

    Article  CAS  PubMed  Google Scholar 

  25. Nedashkovskaya OI et al (2006) Arenibacter palladensis sp. nov., a novel marine bacterium isolated from the green alga Ulva fenestrata, and emended description of the genus Arenibacter. Int J Syst Evol Microbiol 56:155–160. https://doi.org/10.1099/ijs.0.63893-0

    Article  CAS  PubMed  Google Scholar 

  26. Nedashkovskaya OI, Vancanneyt M, De Vos P, Kim SB, Lee MS, Mikhailov VV (2007) Maribacter polysiphoniae sp. nov., isolated from a red alga. Int J Syst Evol Microbiol 57:2840–2843. https://doi.org/10.1099/ijs.0.65181-0

    Article  CAS  PubMed  Google Scholar 

  27. Nedashkovskaya OI, Suzuki M, Lee J-S, Lee KC, Shevchenko LS, Mikhailov VV (2009) Pseudozobellia thermophila gen. nov., sp. nov., a bacterium of the family Flavobacteriaceae, isolated from the green alga Ulva fenestrata. Int J Syst Evol Microbiol 59:806–810. https://doi.org/10.1099/ijs.0.004143-0

    Article  CAS  PubMed  Google Scholar 

  28. Nedashkovskaya OI, Kukhlevskiy AD, Zhukova NV (2013) Polaribacter reichenbachii sp. nov.: a new marine bacterium associated with the green alga Ulva fenestrata. Curr Microbiol 66:16–21. https://doi.org/10.1007/s00284-012-0200-x

    Article  CAS  PubMed  Google Scholar 

  29. Nedashkovskaya OI, Balabanova LA, Zhukova NV, Kim S-J, Bakunina IY, Rhee S-K (2014) Flavobacterium ahnfeltiae sp. nov., a new marine polysaccharide-degrading bacterium isolated from a Pacific red alga. Arch Microbiol 196:745–752. https://doi.org/10.1007/s00203-014-1010-2

    Article  CAS  PubMed  Google Scholar 

  30. Park S, Yoon J-H (2013) Winogradskyella undariae sp. nov., a member of the family Flavobacteriaceae isolated from a brown algae reservoir. Antonie van Leeuwenhoek 104:619–626. https://doi.org/10.1007/s10482-013-9968-3

    Article  CAS  PubMed  Google Scholar 

  31. Park SC et al (2009) Aequorivita capsosiphonis sp. nov., isolated from the green alga Capsosiphon fulvescens, and emended description of the genus Aequorivita. Int J Syst Evol Microbiol 59:724–728. https://doi.org/10.1099/ijs.0.004119-0

    Article  CAS  PubMed  Google Scholar 

  32. Park S, Jung Y-T, Yoon J-H (2013a) Algibacter miyuki sp. nov., a member of the family Flavobacteriaceae isolated from leachate of a brown algae reservoir. Antonie van Leeuwenhoek 104:253–260. https://doi.org/10.1007/s10482-013-9944-y

    Article  CAS  PubMed  Google Scholar 

  33. Park S, Lee J-S, Lee K-C, Yoon J-H (2013b) Algibacter undariae sp. nov., isolated from a brown algae reservoir. Int J Syst Evol Microbiol 63:3704–3709. https://doi.org/10.1099/ijs.0.049734-0

    Article  CAS  PubMed  Google Scholar 

  34. Park S, Lee J-S, Lee K-C, Yoon J-H (2013c) Formosa undariae sp. nov., isolated from a reservoir containing the brown algae Undaria pinnatifida. Int J Syst Evol Microbiol 63:4130–4135. https://doi.org/10.1099/ijs.0.053157-0

    Article  CAS  PubMed  Google Scholar 

  35. Park S, Yoshizawa S, Muramatsu Y, Nakagawa Y, Yokota A, Kogure K (2013d) Aureicoccus marinus gen. nov., sp. nov., a member of the family Flavobacteriaceae, isolated from seawater. Int J Syst Evol Microbiol 63:1885–1890. https://doi.org/10.1099/ijs.0.045104-0

    Article  CAS  PubMed  Google Scholar 

  36. Park S, Park J-M, Jung Y-T, Kang C-H, Yoon J-H (2015a) Lacinutrix undariae sp. nov., isolated from a brown algae reservoir. Int J Syst Evol Microbiol 65:2696–2701. https://doi.org/10.1099/ijs.0.000325

    Article  CAS  PubMed  Google Scholar 

  37. Park S, Park JM, Jung YT, Lee KH, Yoon JH (2015b) Polaribacter undariae sp. nov., isolated from a brown alga reservoir. Int J Syst Evol Microbiol 65:1679–1685. https://doi.org/10.1099/ijs.0.000157

    Article  CAS  PubMed  Google Scholar 

  38. Qi F, Huang Z, Lai Q, Li D, Shao Z (2016) Kordia ulvae sp. nov., a bacterium isolated from the surface of green marine algae Ulva sp. Int J Syst Evol Microbiol 66:2623–2628. https://doi.org/10.1099/ijsem.0.001098

    Article  CAS  PubMed  Google Scholar 

  39. Sasser M (1990) Identification of bacteria by gas chromatography of cellular fatty acids. USFCC Newsl 20:16

    Google Scholar 

  40. 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 Evol Microbiol 44:846–849

    Article  CAS  Google Scholar 

  41. 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 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tindall BJ, Sikorski J, Smibert RA, Krieg NR (2007) Phenotypic characterization and the principles of comparative systematics. In: Reddy CA, Beveridge TJ, Breznak JA, Marzluf G, Schmidt TM, Snyder LR (eds) Methods for general and molecular microbiology. American Society of Microbiology, Washington, DC, pp 330–393

    Google Scholar 

  43. Weerawongwiwat V, Kang H, Jung MY, Kim W (2012) Maribacter chungangensis sp. nov., isolated from a green seaweed, and emended descriptions of the genus Maribacter and Maribacter arcticus. Int J Syst Evol Microbiol 63:2553–2558. https://doi.org/10.1099/ijs.0.039628-0

    Article  CAS  PubMed  Google Scholar 

  44. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yoon B-J, Oh D-C (2012) Spongiibacterium flavum gen. nov., sp. nov., a member of the family Flavobacteriaceae isolated from the marine sponge Halichondria oshoro, and emended descriptions of the genera Croceitalea and Flagellimonas. Int J Syst Evol Microbiol 62:1158–1164. https://doi.org/10.1099/ijs.0.027243-0

    Article  CAS  PubMed  Google Scholar 

  46. Yoon J, Adachi K, Kasai H (2014) Citreitalea marina gen. nov., sp. nov., a novel member of the family Flavobacteriaceae isolated from a marine red alga and emended description of the genus Gangjinia. Antonie van Leeuwenhoek 106:261–269. https://doi.org/10.1007/s10482-014-0190-8

    Article  CAS  PubMed  Google Scholar 

  47. Yoon J, Oku N, Kasai H (2015) Wenyingzhuangia gracilariae sp. nov., a novel marine bacterium of the phylum Bacteroidetes isolated from the red alga Gracilaria vermiculophylla. Antonie van Leeuwenhoek 107:1607–1613. https://doi.org/10.1007/s10482-015-0456-9

    Article  CAS  PubMed  Google Scholar 

  48. Yoon J, Adachi K, Kasai H (2016a) Spongiimicrobium salis gen. nov., sp. nov., a bacterium of the family Flavobacteriaceae isolated from a marine sponge. Arch Microbiol 198:663–670. https://doi.org/10.1007/s00203-016-1227-3

    Article  CAS  PubMed  Google Scholar 

  49. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2016b) Introducing EzBioCloud: a taxonomically united database of 16S rRNA and whole genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Google Scholar 

  50. Yoon J, Yasumoto-Hirose M, Kasai H (2017) Coraliitalea coralii gen. nov., sp. nov., a marine bacterium of the family Flavobacteriaceae isolated from the hard coral Galaxea fascicularis. Curr Microbiol 1:1. https://doi.org/10.1007/s00284-017-1403-y

    CAS  Article  Google Scholar 

  51. Yu Y, Li H-R, Zeng Y-X, Sun K, Chen B (2012) Pricia antarctica gen. nov., sp. nov., a member of the family Flavobacteriaceae, isolated from Antarctic intertidal sediment. Int J Syst Evol Microbiol 62:2218–2223. https://doi.org/10.1099/ijs.0.037515-0

    Article  PubMed  Google Scholar 

  52. Zhang GI, Hwang CY, Kang S-H, Cho BC (2009) Maribacter antarcticus sp. nov., a psychrophilic bacterium isolated from a culture of the Antarctic green alga Pyramimonas gelidicola. Int J Syst Evol Microbiol 59:1455–1459. https://doi.org/10.1099/ijs.0.006056-0

    Article  CAS  PubMed  Google Scholar 

  53. Zhang Y-J et al (2017) Euzebyella marina sp. nov., isolated from seawater. Int J Syst Evol Microbiol 67:920–924. https://doi.org/10.1099/ijsem.0.001712

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We are grateful to the Marine Culture Collection of China for analysing the genome of the type strain.

Funding

This work was supported by the open task of Qingdao National Laboratory for Marine Science and Technology (QNLM2016ORP0311), the National Key Research and Development Program of China (2016YFA0601402), the CNOOC Tianjin project (CNOOC-KJ 125 FZDXM 00TJ 001-2014) and Natural Science Foundation of China (no. 41876174, 31700104). This study is a contribution to the international IMBER project.

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YZ: Conception or design of the work. ZZ, ZH, LT and ZW: Data collection. YZ and ZZ: Data analysis and interpretation. ZZ: Drafting the article. YZ: Critical revision of the article. ZZ, ZH, LT, ZW and YZ: Final approval of the version to be published. ZZ and ZH: Revising the manuscript.

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Correspondence to Yongyu Zhang.

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The GenBank accession numbers for the 16S rRNA gene and the genome sequences of Ulvibacterium marinum CCMM003T are KY060010 and RBCJ01000000, respectively.

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Zhang, Z., Hu, Z., Tang, L. et al. Ulvibacterium marinum gen. nov., sp. nov., a novel marine bacterium of the family Flavobacteriaceae, isolated from a culture of the green alga Ulva prolifera. Antonie van Leeuwenhoek 112, 1077–1085 (2019). https://doi.org/10.1007/s10482-019-01239-x

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Keywords

  • Polyphasic taxonomy
  • Ulvibacterium marinum gen. nov.
  • Ulva prolifera