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Micrococcus lacusdianchii sp. nov., an attached bacterium inhibited by metabolites from its symbiotic algae

The Journal of Antibiotics volume 77, pages 163–169 (2024)Cite this article

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Abstract

A novel actinobacterial strain, designated as JXJ CY 30 T, was isolated from the phycosphere of Microcystis aeruginosa FACHB-905 (Maf) collected from Lake Dianchi, China. The strain was a Gram-stain-positive, aerobic and coccus-shaped actinobacterium. It had alanine, glutamic acid, aspartic acid, and lysine in the peptidoglycan, and mannose, ribose and arabinose in its cell wall sugars, anteiso-C15:0 and iso-C15:0 as the main cellular fatty acids, MK-7 and MK-8 as the major respiratory quinones, and phosphatidylglycerol, diphosphatidylglycerol, phosphatidylinositol, glycolipid, and an unidentified phospholipid as the polar lipids. The DNA G + C content was 73.08%. Its 16 S rRNA gene sequence shared 99.14%, and 98.75% similarities with Micrococcus flavus DSM 19079 T and M. porci KD337-16T, respectively, and ≤98.41% similarities with other type strains of the genus Micrococcus. It formed independent clade with M. flavus DSM 19079 T on the phylogenetic trees. The digital DNA-DNA hybridization and average nucleotide identity values between strain JXJ CY 30 T and M. flavus DSM 19079 T and M. porci KD337-16T were 48.0% and 92.1%, 25.5% and 83.2%, respectively. These data above indicated that strain JXJ CY 30 T represented a new species of the genus Micrococcus, and the species epithet is proposed as Micrococcus lacusdianchii sp. nov. (type strain JXJ CY 30 T = KCTC 49378 T = CGMCC 1.17508 T). Strain JXJ CY 30 T can potentially provide Maf with various nutrients such as available phosphorus and nitrogen, plant hormones, various vitamins and carotenoids for growth, while it was inhibited by metabolites from its symbiotic algae Maf.

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References

  1. Rajasekhar P, Fan L, Nguyen T, Roddick FA. A review of the use of sonication to control cyanobacterial blooms. Water Res. 2012;46:4319–29.

    Article  PubMed  CAS  Google Scholar 

  2. Dawson RM. The toxicology of microcystins. Toxicon. 1998;36:953–62.

    Article  PubMed  CAS  Google Scholar 

  3. Pichardo S, Jos A, Zurita JL, Salguero M, Cameán AM, Repetto G. Acute and subacute toxic effects produced by microcystin-YR on the fish cell lines RTG-2 and PLHC-1. Toxicol Vitr. 2007;21:1460–7.

    Article  CAS  Google Scholar 

  4. Lin W, Hung TC, Kurobe T, Wang Y, Yang P. Microcystin-induced immunotoxicity in fishes: a scoping review. Toxins. 2021;13:765.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Vasconcelos VM, Sivonen K, Evans WR, Carmichael WW, Namikoshi M. Hepatotoxic microcystin diversity in cyanobacterial blooms collected in Portuguese freshwaters. Water Res. 1996;30:2377–84.

    Article  CAS  Google Scholar 

  6. Liu Y, Gao B, Yue Q, Guan Y, Wang Y, Huang L. Influences of two antibiotic contaminants on the production, release and toxicity of microcystins. Ecotox Environ Saf. 2012;77:79–87.

    Article  CAS  Google Scholar 

  7. Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS. Algae-bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv. 2016;34:14–29.

    Article  PubMed  CAS  Google Scholar 

  8. Kouzuma A, Watanabe K. Exploring the potential of algae/bacteria interactions. Curr Opin Biotech. 2015;33:125–9.

    Article  PubMed  CAS  Google Scholar 

  9. Cooper MB, Smith AG. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Curr Opin Plant Biol. 2015;26:147–53.

    Article  PubMed  Google Scholar 

  10. Parveen B, Ravet V, Djediat C, Mary I, Quiblier C, Debroas D, Humbert J-F. Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ Microbiol Rep. 2013;5:716–24.

    Article  PubMed  CAS  Google Scholar 

  11. Shi L, Cai Y, Kong F, Yu Y. Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environ Microbiol Rep. 2012;4:669–78.

    Article  PubMed  CAS  Google Scholar 

  12. Casamatta D, Wickstrom C. Sensitivity of two distinct bacterioplankton communities to exudates from the cyanobacterium Microcystis aeruginosa. Micro Ecol. 2000;41:64–73.

    Article  ADS  Google Scholar 

  13. Niu Y, Shen H, Chen J, Xie P, Yang X, Tao M, Ma Z, Qi M. Phytoplankton community succession shaping bacterioplankton community composition in Lake Taihu, China. Water Res. 2011;45:4169–82.

    Article  PubMed  CAS  Google Scholar 

  14. Shi L, Cai Y, Yang H, Xing P, Li P, Kong L, Kong F. Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. J Environ Sci. 2009;21:1581–90.

    Article  Google Scholar 

  15. Dziallas C, Grossart HP. Temperature and biotic factors influence bacterial communities associated with the cyanobacterium Microcystis sp. Environ Microbiol. 2011;13:1632–41.

    Article  PubMed  Google Scholar 

  16. Zhao G, Du J, Jia Y, Lv Y, Han G, Tian X. The importance of bacteria in promoting algal growth in eutrophic lakes with limited available phosphorus. Ecol Eng. 2012;42:107–11.

    Article  CAS  Google Scholar 

  17. Zhang B, Salam N, Cheng J, Li H, Yang J, Zha D, Zhang Y, Ai M, Hozzein WaelN, Li W. Modestobacter lacusdianchii sp. nov., a phosphate-solubilizing actinobacterium with ability to promote Microcystis growth. Plos One. 2016;11:e0161069.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Cirri E, Pohnert G. Algae-bacteria interactions that balance the planktonic microbiome. N Phytol. 2019;223:100–6.

    Article  Google Scholar 

  19. Hoke AK, Reynoso G, Smith MR, Gardner MI, Lockwood DJ, Gilbert NE, Wilhelm SW, Becker IR, Brennan GJ, Crider KE, Farnan SR, Mendoza V, Poole AC, Zimmerman ZP, Utz LK, Wurch LL, Steffen MM. Genomic signatures of Lake Erie bacteria suggest interaction in the Microcystis phycosphere. Plos One. 2021;16:e0257017.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Seyedsayamdost MR, Case RJ, Kolter R, Clardy J. The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat Chem. 2011;3:331–5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Deng J, Li J, Guan Z, Hu B, Zhao L, Li P. Effect of attached bacteria of carbonic anhydrase on the growth of Microcystis aeruginosa. J Lake Sci. 2012;24:429–35.

    Article  CAS  Google Scholar 

  22. Li H, Zhang B, Yang J, Zha D, Guo Q, Shi X, Guo J. Cyanobacteria-lytic activity of Streptomyces eurocidicus JXJ 0089 against Microcystis aeruginosa. Jiangsu J Agr Sci. 2015;31:1037–44.

    Google Scholar 

  23. Liu LP.Characteristics of blue algal bloom in Dianchi Lake and analysis on its cause.Res Environ Sci. 1999;12:36–37.

    Google Scholar 

  24. Cohn F. Untersuchungen über Bakterien. Beitr Biol Pflanz. 1872;1:127–244.

    Google Scholar 

  25. Stackebrandt E, Koch C, Gvozdiak O, Schumann P. Taxonomic dissection of the genus Micrococcus: Kocuria gen. nov., Nesterenkonia gen. nov., Kytococcus gen. nov., Dermacoccus gen. nov., and Micrococcus Cohn 1872 gen. emend. Int J Syst Bacteriol. 1995;45:682–92.

    Article  PubMed  CAS  Google Scholar 

  26. Wieser M, Denner EB, Kämpfer P, Schumann P, Tindall B, Steiner U, Vybiral D, Lubitz W, Maszenan AM, Patel BKC, Seviour RJ, Radax C, Busse HJ. Emended descriptions of the genus Micrococcus, Micrococcus luteus (Cohn 1872) and Micrococcus lylae (Kloos et al. 1974). Int J Syst Evol Microbiol. 2002;52:629–37.

    Article  PubMed  CAS  Google Scholar 

  27. Huang CH, Wang CL, Liou JS, Lee AY, Blom J, Huang L, Watanabe K. Reclassification of Micrococcus aloeverae and Micrococcus yunnanensis as later heterotypic synonyms of Micrococcus luteus. Int J Syst Evol Microbiol. 2019;69:3512–8.

    Article  PubMed  CAS  Google Scholar 

  28. Shirling EB, Gottlieb D. Methods for characterization of Streptomyces species. Int J Syst Bacteriol. 1966;16:313–40.

    Article  Google Scholar 

  29. Allen MM. Simple conditions for growth of unicellular blue-green algae on plates. J Phycol 1968;4:1–4.

    Article  PubMed  CAS  Google Scholar 

  30. Dong X, Cai M Manual of systematic identification of common bacteria. Beijing: Science Press, 2001. p 349–89.

  31. Minnikin DE, Collins MD, Goodfellow M. Fatty acid and polar lipid composition in the classification of Cellulomonas, Oerskovia and related taxa. J Appl Bacteriol. 1997;47:87–95.

    Article  Google Scholar 

  32. Collins MD, Pirouz T, Goodfellow M. Distribution of menaquinones in actinomycetes and corynebacteria. J Gen Microbiol. 1977;100:221–30.

    Article  PubMed  CAS  Google Scholar 

  33. Tamaoka J, Katayama-Fujimura Y, Kuraishi H. Analysis of bacterial menaquinone mixtures by high performance liquid chromatography. J Appl Bacteriol. 1983;54:31–36.

    Article  CAS  Google Scholar 

  34. Tang S, Wang Y, Chen Y, Lou K, Cao L, Xu L, Li W. Zhihengliuella alba sp. nov., and emended description of the genus Zhihengliuella. Int J Syst Evol Microbiol. 2009;59:2025–32.

    Article  PubMed  CAS  Google Scholar 

  35. Zhang B, Salam N, Cheng J, Xiao M, Li H, Yang J, Zha D, Li W. Citricoccus lacusdiani sp. nov., an actinobacterium promoting Microcystis growth with limited soluble phosphorus. Antonie Van Leeuwenhoek. 2016;109:1457–65.

    Article  PubMed  CAS  Google Scholar 

  36. Saitou N, Nei M. The neighbor–joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406–42.

    PubMed  CAS  Google Scholar 

  37. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17:368–76.

    Article  ADS  PubMed  CAS  Google Scholar 

  38. Fitch WM. Toward defining the course of evolution: minimum change for a specific tree topology. Syst Biol. 1971;20:406–16.

    Article  Google Scholar 

  39. 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. 2011;28:2731–9.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91.

    Article  PubMed  Google Scholar 

  41. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. 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. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–77.

    Article  MathSciNet  PubMed  PubMed Central  CAS  Google Scholar 

  43. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol. 2012;13:R56.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Massouras A, Hens K, Gubelmann C, Uplekar S, Decouttere F, Rougemont J, Cole ST, Bart Deplancke B. Primer-initiated sequence synthesis to detect and assemble structural variants. Nat Methods. 2010;7:485–6.

    Article  PubMed  CAS  Google Scholar 

  45. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    Article  PubMed  CAS  Google Scholar 

  46. Bland C, Ramsey TL, Sabree F, Lowe M, Brown K, Kyrpides NC, Hugenholtz P. CRISPR Recognition Tool (CRT): a tool for automatic detection of clustered regularly interspaced palindromic repeats. BMC Bioinform. 2007;8:209.

    Article  Google Scholar 

  47. Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence–based species delimitation with confidence intervals and improved distance functions. BMC Bioinform. 2013;14:60.

    Article  Google Scholar 

  48. Zhang B, Ding Z, Li H, Mou X, Zhang Y, Yang J, Zhou E, Li W. Algicidal activity of Streptomyces eurocidicus JXJ-0089 metabolites and their effects on Microcystis physiology. Appl Environ Micro. 2016;82:5132–43.

    Article  ADS  CAS  Google Scholar 

  49. Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, Meyer SD, Trujillo ME. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol. 2018;68:461–6.

    Article  PubMed  CAS  Google Scholar 

  50. Zhu C, Zhang J, Wang X, Yang Y, Chen N, Lu Z, Ge Q, Jiang R, Zhang X, Yang Y, Chen T. Responses of cyanobacterial aggregate microbial communities to algal blooms. Water Res. 2021;196:117014.

    Article  PubMed  CAS  Google Scholar 

  51. Pérez-Carrascal OM, Tromas N, Terrat Y, Moreno E, Giani A, Marques LCB, Fortin N, Shapiro BJ. Single-colony sequencing reveals microbe-by-microbiome phylosymbiosis between the cyanobacterium Microcystis and its associated bacteria. Microbiome. 2021;9:194. –194

    Article  PubMed  PubMed Central  Google Scholar 

  52. Young AJ. The photoprotective role of carotenoids in higher plants. Physiol Plant. 1991;83:702–8.

    Article  CAS  Google Scholar 

  53. Kim M, Shin B, Lee J, Park HY, Park W. Culture-independent and culture-dependent analyses of the bacterial community in the phycosphere of cyanobloom-forming Microcystis aeruginosa. Sci Rep. 2019;9:20416.

    Article  ADS  PubMed  PubMed Central  CAS  Google Scholar 

  54. Xiao Y, Chen J, Chen M, Deng S, Xiong Z, Tian B, Zhang B. Mycolicibacterium lacusdiani sp. nov., an attached bacterium of Microcystis aeruginosa. Front Microbiol. 2022;13:e861291.

    Article  Google Scholar 

  55. Xiao Y, Wang L, Wang X, Chen M, Chen J, Tian B, Zhang B. Nocardioides lacusdianchii sp. nov., an attached bacterium of Microcystis aeruginosa. Antonie Van Leeuwenhoek. 2022;115:141–53.

    Article  PubMed  Google Scholar 

  56. Xiao Y, Chen M, Chen J, Mao L, Peng Y, Gui S, Zhang B. Microbacterium kunmingensis sp. nov., an attached bacterium of Microcystis aeruginosa. J Antibiot. 2022;75:662–70.

    Article  CAS  Google Scholar 

  57. Zhang B, Salam N, Cheng J, Li H, Yang J, Zha D, Guo Q, Li W. Microbacterium lacusdiani sp. nov., a phosphate-solubilizing novel actinobacterium isolated from mucilaginous sheath of Microcystis. J Antibiot. 2017;70:147–51.

    Article  Google Scholar 

  58. Østensvik Ø, Skulberg OM, Underdal B, Hormazabal V. Antibacterial properties of extracts from selected planktonic freshwater cyanobacteria—a comparative study of bacterial bioassays. J Appl Microbiol. 1998;84:1117–24.

    Article  PubMed  Google Scholar 

  59. Valdor R, Aboal M. Effects of living cyanobacteria, cyanobacterial extracts and pure microcystins on growth and ultrastructure of microalgae and bacteria. Toxicon. 2007;49:769–79.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by National Natural Science Foundation of China (NO. 32360028), and Programs of the Education Department of Jiangxi Province of China (GJJ211837).

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  1. These authors contributed equally: Le Wang, Yao Xiao

Authors and Affiliations

  1. College of Pharmacy and Life Science, Jiujiang University, Jiujiang, 332005, China

    Le Wang, Yao Xiao, Wenxin Lai, Ru Jia, Qinglin Deng, Xin Wang, Hongqiu Shi, Yiwen Yang & Binghuo Zhang

  2. Jiujiang Key Laboratory for the Development and Utilization of Traditional Chinese Medicine resources in Northwest Jiangxi, Jiujiang, China

    Binghuo Zhang

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Contributions

BZ designed the experiments. LW, YX, WL, RJ, QD and XW performed the experiments. LW, YX, HS, YY and BZ analyzed the data, and drafted and revised the manuscript. All authors reviewed and approved the final version of the paper.

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Correspondence to Yiwen Yang or Binghuo Zhang.

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Wang, L., Xiao, Y., Lai, W. et al. Micrococcus lacusdianchii sp. nov., an attached bacterium inhibited by metabolites from its symbiotic algae. J Antibiot 77, 163–169 (2024). https://doi.org/10.1038/s41429-023-00690-3

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