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Strain-specific responses of toxic and non-toxic Microcystis aeruginosa to exudates of heterotrophic bacteria

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Abstract

Although the cyanobacterium Microcystis is colonial during water blooms, isolated Microcystis strains become unicellular in culture. Studies indicate that heterotrophic bacteria can promote Microcystis colonies in culture, but little is known about the underlying mechanism or how widespread it is among bacteria. This study investigated the identity and colony-promoting effects of bacteria isolated from the 2014 Microcystis bloom in Lake Erie. Isolates were classified by their 16S rRNA gene sequences. Toxic and non-toxic cultures of M. aeruginosa were exposed to exudates of bacterial isolates, and their morphology, polysaccharide content, and reflectance spectra were compared to those of M. aeruginosa control cultures. Six isolates belonging to three genera enhanced the frequency or size of M. aeruginosa colonies in cultures where a dialysis barrier prevented direct contact between heterotrophic cells and M. aeruginosa cells. Toxic and non-toxic M. aeruginosa strains differed in how their morphology and optical properties responded to treatment. This study demonstrates that heterotrophic bacteria can promote colonial morphology in Microcystis without making physical contact with the Microcystis cells, as well as the first to indicate that toxic and non-toxic strains of the same morphospecies have different morphological and optical responses.

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References

  • Altschup, S. F., W. Gish, W. Miller, E. W. Myers & D. J. Lipman, 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403–410.

    Google Scholar 

  • Auger, S., E. Krin, S. Aymerich & M. Gohar, 2006. Autoinducer 2 affects biofilm formation by Bacillus cereus. Applied and Environmental Microbiology 72: 937–941.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Biswa, P. & M. Doble, 2013. Production of acylated homoserine lactone by Gram-positive bacteria isolated from marine water. FEMS Microbiology Letters 343: 34–41.

    CAS  PubMed  Google Scholar 

  • Bolch, C. J. S. & S. I. Blackburn, 1996. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kutz. Journal of Applied Phycology 8: 5–13.

    Google Scholar 

  • Burkert, U., P. Hyenstrand, S. Drakare & P. Blomqvist, 2001. Effects of the mixotrophic flagellate Ochromonas sp. on colony formation in Microcystis aeruginosa. Aquatic Ecology 35: 11–17.

    Google Scholar 

  • Case, R. J., M. Labbate & S. Kjelleberg, 2008. AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME Journal 2: 345.

    CAS  PubMed  Google Scholar 

  • Curran, J., 2018. Hotelling: hotelling’s T^2 test and variants. R package version 1.0-5. https://CRAN.R-project.org/package=Hotelling.

  • Davis, T. W., D. L. Berry, G. L. Boyer & C. J. Gobler, 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8: 715–725.

    CAS  Google Scholar 

  • De Maesschalck, R., D. Jouan-Rimbaud & D. L. Massart, 2000. The mahalanobis distance. Chemometrics and Intelligent Laboratory Systems 50: 1–18.

    Google Scholar 

  • Dinno, A., 2017. dunn.test: Dunn’s test of multiple comparisons using rank sums. R package version 1.3.5. https://CRAN.R-project.org/package=dunn.test.

  • D’Orazio, M., 2019. StatMatch: statistical matching or data fusion. R package version 1.3.0. https://CRAN.R-project.org/package=StatMatch.

  • Dubois, M., K. A. Gilles, J. K. Hamilton, P. A. Roberts & F. Smith, 1956. Phenol sulphuric acid method for carbohydrate determination. Annals of Chemistry 28: 350–359.

    CAS  Google Scholar 

  • Dunn, O. J., 1961. Multiple comparisons among means. Journal of the American Statistical Association 56: 52–64.

    Google Scholar 

  • Fernandes, M. D. S., L. M. R. Esper, D. Y. Kabuki & A. Y. Kuaye, 2018. Quorum sensing in Enterococcus faecium, Enterococcus faecalis and Bacillus cereus strains isolated from ricotta processing. Ciênc Rural. https://doi.org/10.1590/0103-8478cr20161111.

    Article  Google Scholar 

  • Francy, D. S., J. L. Graham, E. A. Stelzer, C. D. Ecker, A. M. G. Brady, P. Struffolino & K. A. Loftin, 2015. Water quality, cyanobacteria, and environmental factors and their relations to microcystin concentrations for use in predictive models at Ohio Lake Erie and inland lake recreational sites, 2013–14: U.S. Geological Survey Scientific Investigations Report 2015–5120, 58 p. http://dx.doi.org/10.3133/sir20155120.

  • Gan, N., Y. Xiao, L. Zhu, Z. Wu, J. Liu, C. Hu & L. Song, 2012. The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environmental Microbiology 14: 730–742.

    CAS  PubMed  Google Scholar 

  • Gantt, E., 1975. Phycobilisomes: light-harvesting pigment complexes. Bioscience 25: 781–788.

    CAS  Google Scholar 

  • Ha, K., M. H. Jang & N. Takamura, 2004. Colony formation in planktonic algae induced by zooplankton culture media filtrate. Journal of Freshwater Ecology 19: 9–16.

    Google Scholar 

  • Haas, D. & G. Défago, 2005. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 3: 307.

    CAS  PubMed  Google Scholar 

  • Hotelling, H., 1951. A generalized T test and measure of multivariate dispersion. In Proceedings of the Second Berkeley Symposium on Mathematical Statistics and Probability. The Regents of the University of California.

  • Jarvis, A. C., R. C. Hart & S. Combrink, 1987. Zooplankton feeding on size fractionated Microcystis colonies and Chlorella in a hypertrophic lake (Hartbeespoort Dam, South Africa): implications to resource utilization and zooplankton succession. Journal of Plankton Research 9: 1231–1249.

    Google Scholar 

  • Johnson, S. G., 2016. The NLopt nonlinear-optimization package, http://abinitio.mit.edu/nlopt.

  • Jones, M. B. & M. J. Blaser, 2003. Detection of a luxS-signaling molecule in Bacillus anthracis. Infection and Immunity 71: 3914–3919.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joung, S. H., H. M. Oh, S. R. Ko & C. Y. Ahn, 2011. Correlations between environmental factors and toxic and non-toxic Microcystis dynamics during bloom in Daechung Reservoir, Korea. Harmful Algae 10: 188–193.

    Google Scholar 

  • Juhas, M., L. Eberl & B. Tümmler, 2005. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environmental Microbiology 7: 459–471.

    CAS  PubMed  Google Scholar 

  • Kardinaal, W. E. A., I. Janse, M. P. Kamst-van Agterveld, M. Meima, J. Snoek, L. R. Mur, J. Huisman, G. Zwart & P. M. Visser, 2007. Microcystis genotype succession in relation to microcystin concentrations in freshwater lakes. Aquatic Microbial Ecology 48: 1–12.

    Google Scholar 

  • Kehr, J. C., Y. Zilliges, A. Springer, M. D. Disney, D. D. Ratner, C. Bouchier, P. H. Seeberger, N. Tandeau de Marsac & E. Dittmann, 2006. A mannan binding lectin is involved in cell–cell attachment in a toxic strain of Microcystis aeruginosa. Molecular Microbiology 9: 893–906.

    Google Scholar 

  • Keller, L. & M. G. Surette, 2006. Communication in bacteria: an ecological and evolutionary perspective. Nature Reviews Microbiology 4: 249.

    CAS  PubMed  Google Scholar 

  • Kruskal, W. H. & W. A. Wallis, 1952. Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association 47: 583–621.

    Google Scholar 

  • Kumar, S., K. Tamura & M. Nei, 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefs in Bioinformatics 5: 150–163.

    CAS  Google Scholar 

  • Kumar, S., G. Stecher & K. Tamura, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kurmayer, R., G. Christiansen & I. Chorus, 2003. The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee. Applied and Environmental Microbiology 69: 787–795.

    CAS  PubMed  PubMed Central  Google Scholar 

  • La Duc, M. T., S. Osman, P. Vaishampayan, Y. Piceno, G. Andersen, J. A. Spry & K. Venkateswaran, 2009. Comprehensive census of bacteria in clean rooms by using DNA microarray and cloning methods. Applied and Environmental Microbiology 75: 6559–6567.

    PubMed  PubMed Central  Google Scholar 

  • Lane, D. J., B. Pace, G. J. Olsen, D. A. Stahl, M. L. Sogin & N. R. Pace, 1985. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences 82: 6955–6959.

    CAS  Google Scholar 

  • Lawton, L. A., C. Edwards & G. A. Codd, 1994. Extraction and high-performance liquid chromatographic method for the determination of microcystins in raw and treated waters. Analyst 119: 1525–1530.

    CAS  PubMed  Google Scholar 

  • Lee, J., & L. Zhang, 2015. The hierarchy quorum sensing network in Pseudomonas aeruginosa. Protein and Cell 6: 26–41.

    CAS  PubMed  Google Scholar 

  • Leitão, E., K. A. Ger & R. Panosso, 2018. Selective grazing by a tropical copepod (Notodiaptomus iheringi) facilitates Microcystis dominance. Frontiers in Microbiology 9: 301.

    PubMed  PubMed Central  Google Scholar 

  • Li, M., W. Zhu, L. Guo, J. Hu, H. Chen & M. Xiao, 2016. To increase size or decrease density? Different Microcystis species has different choice to form blooms. Scientific Reports 6: 37056.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lombardía, E., A. J. Rovetto, A. L. Arabolaza & R. R. Grau, 2006. A LuxS-dependent cell-to-cell language regulates social behavior and development in Bacillus subtilis. Journal of Bacteriology 188: 4442–4452.

    PubMed  PubMed Central  Google Scholar 

  • Lürling, M., F. Van Oosterhout & E. Faassen, 2017. Eutrophication and warming boost cyanobacterial biomass and microcystins. Toxins 9: 64.

    PubMed Central  Google Scholar 

  • Mahalanobis, P. C., 1936. On the generalised distance in statistics. Proceedings of the National Institute of Science of India 12: 49–55.

    Google Scholar 

  • Molohon, K. J., J. O. Melby, J. Lee, B. S. Evans, K. L. Dunbar, S. B. Bumpus, N. L. Kelleher & D. A. Mitchell, 2011. Structure determination and interception of biosynthetic intermediates for the plantazolicin class of highly discriminating antibiotics. ACS Chemical Biolology 6: 1307–1313.

    CAS  Google Scholar 

  • Muyzer, G., E. C. De Waal & A. G. Uitterlinden, 1993. Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59: 695–700.

    CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.

    Google Scholar 

  • Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.

    CAS  PubMed  Google Scholar 

  • Paerl, H. W. & V. J. Paul, 2012. Climate change: links to global expansion of harmful cyanobacteria. Water Research 46: 1349–1363.

    CAS  PubMed  Google Scholar 

  • Passos da Silva, D., M. C. Schofield, M. R. Parsek & B. S. Tseng, 2017. An update on the sociomicrobiology of quorum sensing in gram-negative biofilm development. Pathogens 6: 51.

    PubMed Central  Google Scholar 

  • Pathak, R., R. Kumar & H. K. Gautam, 2013. Cross-species induction and enhancement of antimicrobial properties in response to gamma irradiation in Exiguobacterium sp. HKG 126. Indian Journal of Microbiology 53: 130–136.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Plude, J. L., D. L. Parker, O. J. Schommer, R. J. Timmerman, S. A. Hagstrom, J. M. Joers & R. Hnasko, 1991. Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae C3-40. Applied and Environmental Microbiology 57: 1696–1700.

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team, 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Raaijmakers, J. M., M. Vlami & J. T. De Souza, 2002. Antibiotic production by bacterial biocontrol agents. Antonie van Leeuwenhoek 81: 537.

    CAS  PubMed  Google Scholar 

  • Reasoner, D. J. & E. E. Geldreich, 1985. A new medium for the enumeration and subculture of bacteria from potable water. Applied and Environmental Microbiology 49: 1–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reynolds, C. S., G. H. M. Jaworski, H. A. Cmiech & G. F. Leedale, 1981. On the annual cycle of the blue-green alga Microcystis aeruginosa Kütz. emend. Elenkin. Philosophical Transactions of the Royal Society of London Series B 293: 419–477.

    Google Scholar 

  • Rickard, A. H., R. J. Paler, D. S. Blehert, S. R. Campagna, M. F. Semmelhack, P. G. Egland, B. L. Bassler & P. E. Kolenbrander, 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Molecular Microbiology 60: 1446–1456.

    CAS  PubMed  Google Scholar 

  • Ryan, R. P. & J. M. Dow, 2008. Diffusible signals and interspecies communication in bacteria. Microbiology 154: 1845–1858.

    CAS  PubMed  Google Scholar 

  • Sedmak, B. & T. Eleršek, 2006. Microcystins induce morphological and physiological changes in selected representative phytoplanktons. Microbial Ecology 51: 508–515.

    CAS  PubMed  Google Scholar 

  • Shamsollahi, H. R., M. Alimohammadi, R. Nabizadeh, S. Nazmara, & A. H. Mahvi, 2015. Measurement of microcystin-LR in water samples using improved HPLC method. Global Journal of Health Science 7: 66

    Google Scholar 

  • Shapiro, S. S. & M. B. Wilk, 1965. An analysis of variance test for normality (complete samples). Biometrika 52: 591–611.

    Google Scholar 

  • Shen, H., Y. Niu, P. Xie, M. I. N. Tao & X. I. Yang, 2011. Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biology 56: 1065–1080.

    CAS  Google Scholar 

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan, L. R., P. F. Xia, R. J. Zeng, Q. Li, X. F. Sun & S. G. Wang, 2018. Low-level concentrations of aminoglycoside antibiotics induce the aggregation of cyanobacteria. Environmental Science and Pollution Research. https://doi.org/10.1007/s11356-018-1894-5.

    Article  PubMed  Google Scholar 

  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Gremberghe, I., P. Vanormelingen, B. Vanelslander, K. Van der Gucht, S. D’hondt, L. De Meester & W. Vyverman, 2009. Genotype-dependent interactions among sympatric Microcystis strains mediated by Daphnia grazing. Oikos 118: 1647–1658.

    Google Scholar 

  • Vanderploeg, H. A., J. R. Liebig, W. W. Carmichael, M. A. Agy, T. H. Johengen, G. L. Fahnenstiel & T. F. Nalepa, 2001. Zebra mussel (Dreissena polymorpha) selective filtration promoted toxic Microcystis blooms in Saginaw Bay (Lake Huron) and Lake Erie. Canadian Journal of Fisheries and Aquatic Science 58: 1208–1221.

    CAS  Google Scholar 

  • Wang, W. & M. Sun, 2009. Phylogenetic relationships between Bacillus species and related genera inferred from 16 s rDNA sequences. Brazilian Journal of Microbiology 40: 505–521.

    Google Scholar 

  • Wang, X., B. Qin, G. Gao & H. W. Paerl, 2010. Nutrient enrichment and selective predation by zooplankton promote Microcystis (Cyanobacteria) bloom formation. Journal of Plankton Research 32: 457–470.

    Google Scholar 

  • Wang, W., H. Shen, P. Shi, J. Chen, L. Ni & P. Xie, 2015. Experimental evidence for the role of heterotrophic bacteria in the formation of Microcystis colonies. Journal of Applied Phycolog. https://doi.org/10.1007/s10811-015-0659-5.

    Article  Google Scholar 

  • White, J. D. & O. Sarnelle, 2014. Size-structured vulnerability of the colonial cyanobacterium, Microcystis aeruginosa, to grazing by zebra mussels (Dreissena polymorpha). Freshwater Biology 59: 514–525.

    Google Scholar 

  • White, J. D., R. B. Kaul, L. B. Knoll, A. E. Wilson & O. Sarnelle, 2011. Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnology and Oceanography 56: 1714–1724.

    Google Scholar 

  • Wickham, H., J. Hester & R. Francois, 2016. readr: Read Tabular Data. R package version 1.0.0. https://CRAN.R-project.org/package=readr.

  • Winson, M. K., M. Camara, A. Latifi, M. Foglino, S. R. Chhabra, M. Daykin, M. Bally, V. Chapon, G. P. C. Salmonds, B. W. Bycroft, A. Lazdunski, G. S. A. B. Stewart & P. Williams, 1995. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proceedings of the National Academy of Sciences 92: 9427–9431.

    CAS  Google Scholar 

  • Wu, X. & F. Kong, 2009. Effects of light and wind speed on the vertical distribution of Microcystis aeruginosa colonies of different sizes during a summer bloom. International Review of Hydrobiology 94: 258–266.

    Google Scholar 

  • Xu, H., G. Yu & H. Jiang, 2013. Investigation on extracellular polymeric substances from mucilaginous cyanobacterial blooms in eutrophic freshwater lakes. Chemosphere 93: 75–81.

    CAS  PubMed  Google Scholar 

  • Xue, T., J. Ni, F. Shang, X. Chen & M. Zhang, 2015. Autoinducer-2 increases biofilm formation via an ica-and bhp-dependent manner in Staphylococcus epidermidis RP62A. Microbes and Infection 17: 345–352.

    CAS  PubMed  Google Scholar 

  • Yamamoto, Y., F. K. Shiah & Y. L. Chen, 2011. Importance of large colony formation in bloom-forming cyanobacteria to dominate in eutrophic ponds. Annals de Limnologie-International Journal of Limnology 7: 167–173.

    Google Scholar 

  • Yang, Z. & F. Kong, 2012. Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. Journal of Limnology 71: 5.

    Google Scholar 

  • Yang, Z., F. X. Kong, H. S. Cao & X. L. Shi, 2005. Observation on colony formation of Microcystis aeruginosa induced by filtered lake water under laboratory conditions. Annals de Limnologie-International Journal of Limnology 41: 169–173.

    Google Scholar 

  • Yang, Z., F. Kong, X. Shi, M. Zhang, P. Xing & H. Cao, 2008. Changes in the morphology and polysaccharide content of Microcystis aeruginosa (cyanobacteria) during flagellate grazing. Journal of Phycology 44: 716–720.

    PubMed  Google Scholar 

  • Zhai, C., P. Zhang, F. Shen, C. Zhou & C. Liu, 2012. Does Microcystis aeruginosa have quorum sensing? FEMS Microbiology Letters 336: 38–44.

    CAS  PubMed  Google Scholar 

  • Zhang, P., M. Chen, Y. Zhang, Y. Li, S. Lu & P. Li, 2018. Autoaggregation and adhesion abilities in bacteria associated with colonies of Microcystis. Hydrobiologia 832: 205–216.

    Google Scholar 

  • Zhu, W., M. Li, Y. Luo, X. Dai, L. Guo, M. Xiao, J. Huang & X. Tan, 2014. Vertical distribution of Microcystis colony size in Lake Taihu: its role in algal blooms. Journal of Great Lakes Research 40: 949–955.

    Google Scholar 

  • Zilliges, Y., J. C. Kehr, S. Mikkat, C. Bouchier, N. T. de Marsac, T. Börner & E. Dittmann, 2008. An extracellular glycoprotein is implicated in cell-cell contacts in the toxic cyanobacterium Microcystis aeruginosa PCC 7806. Journal of Bacteriology 190: 2871–2879.

    CAS  PubMed  PubMed Central  Google Scholar 

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This research was funded in part by the Art and Margaret Herrick Memorial Award.

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Akins, L., Ortiz, J. & Leff, L.G. Strain-specific responses of toxic and non-toxic Microcystis aeruginosa to exudates of heterotrophic bacteria. Hydrobiologia 847, 75–89 (2020). https://doi.org/10.1007/s10750-019-04073-4

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