Gene expression in the microbial consortia of colonial Microcystis aeruginosa-a potential buoyant particulate biofilm.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
29
06
2022
received:
14
09
2021
accepted:
07
07
2022
pubmed:
16
7
2022
medline:
20
10
2022
entrez:
15
7
2022
Statut:
ppublish
Résumé
Microcystis spp., notorious bloom-forming cyanobacteria, are often present in colony form in eutrophic lakes worldwide. Uncovering the mechanisms underlying Microcystis colony formation and maintenance is vital to controlling the blooms, but it has long been a challenge. Here, bacterial communities and gene expression patterns of colonial and unicellular forms of one non-axenic strain of Microcystis aeruginosa isolated from Lake Taihu were compared. Evidently, different microbial communities between them were observed through 16S rDNA MiSeq sequencing. Metatranscriptome analyses revealed that transcripts for pathways involved in bacterial biofilm formation, such as biosynthesis of peptidoglycan and arginine by Bacteroidetes, methionine biosynthesis, alginate metabolism, flagellum, and motility, as well as widespread colonization islands by Proteobacteria, were highly enriched in the colonial form. Furthermore, transcripts for nitrogen fixation and denitrification pathways by Proteobacteria that usually occur in biofilms were significantly enriched in the colonial Microcystis. Results revealed that microbes associated with Microcystis colonies play important roles through regulation of biofilm-related genes in colony formation and maintenance. Moreover, Microcystis colony represents a potential 'buoyant particulate biofilm', which is a good model for biofilm studies. The biofilm features of colonial Microcystis throw a new light on management and control of the ubiquitous blooms in eutrophic waters.
Identifiants
pubmed: 35837847
doi: 10.1111/1462-2920.16133
doi:
Substances chimiques
Alginates
0
DNA, Ribosomal
0
Peptidoglycan
0
Arginine
94ZLA3W45F
Methionine
AE28F7PNPL
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4931-4945Informations de copyright
© 2022 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Akins, L., Ortiz, J. & Leff, L.G. (2020) Strain-specific responses of toxic and non-toxic Microcystis aeruginosa to exudates of heterotrophic bacteria. Hydrobiologia, 847, 75-89.
Armitano, J., Mejean, V. & Jourlin-Castelli, C. (2014) Gram-negative bacteria can also form pellicles. Environmental Microbiology Reports, 6, 534-544.
Bernier, S.P., Ha, D.G., Khan, W., Merritt, J.H. & O'Toole, G.A. (2011) Modulation of Pseudomonas aeruginosa surface-associated group behaviors by individual amino acids through c-di-GMP signaling. Research in Microbiology, 162, 680-688.
Bertrand, E.M., Allen, A.E., Dupont, C.L., Norden-Krichmar, T.M., Bai, J., Valas, R.E. et al. (2012) Influence of cobalamin scarcity on diatom molecular physiology and identification of a cobalamin acquisition protein. Proceedings of the National Academy of Sciences of the United States of America, 109, E1762-E1771.
Bucher, T., Oppenheimer-Shaanan, Y., Savidor, A., Bloom-Ackermann, Z. & Kolodkin-Gal, I. (2015) Disturbance of the bacterial cell wall specifically interferes with biofilm formation. Environmental Microbiology Reports, 7, 990-1004.
Chen, Y., Lun, A.T. & Smyth, G.K. (2016) From reads to genes to pathways: differential expression analysis of RNA-Seq experiments using Rsubread and the edgeR quasi-likelihood pipeline. F1000Res, 5, 1438.
Chun, S.-J., Cui, Y., Lee, J.J., Choi, I.-C., Oh, H.-M. & Ahn, C.-Y. (2019) Network analysis reveals succession of Microcystis genotypes accompanying distinctive microbial modules with recurrent patterns. Water Research, 170, 115326.
Cook, K.V., Li, C., Cai, H., Krumholz, L.R., Hambright, K.D., Paerl, H.W. et al. (2020) The global Microcystis interactome. Limnology and Oceanography, 65, S194-S207.
Croft, M.T., Lawrence, A.D., Raux-Deery, E., Warren, M.J. & Smith, A.G. (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature, 438, 90-93.
Dimitriu, T., Lotton, C., Benard-Capelle, J., Misevic, D., Brown, S.P., Lindner, A.B. et al. (2014) Genetic information transfer promotes cooperation in bacteria. Proceedings of the National Academy of Sciences of the United States of America, 111, 11103-11108.
Donlan, R.M. (2002) Biofilms: microbial life on surfaces. Emerging Infectious Diseases, 8, 881-890.
Fenech, M. (2012) Folate (vitamin B9) and vitamin B12 and their function in the maintenance of nuclear and mitochondrial genome integrity. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis, 733, 21-33.
Flemming, H.C. & Wingender, J. (2010) The biofilm matrix. Nature Reviews Microbiology, 8, 623-633.
Flemming, H.C., Wingender, J., Szewzyk, U., Steinberg, P., Rice, S.A. & Kjelleberg, S. (2016) Biofilms: an emergent form of bacterial life. Nature Reviews Microbiology, 14, 563-575.
Franklin, M.J., Nivens, D.E., Weadge, J.T. & Howell, P.L. (2011) Biosynthesis of the Pseudomonas aeruginosa extracellular polysaccharides, alginate, Pel, and Psl. Frontiers in Microbiology, 2, 167.
Gan, N., Xiao, Y., Zhu, L., Wu, Z., Liu, J., Hu, C. et al. (2012) The role of microcystins in maintaining colonies of bloom-forming Microcystis spp. Environmental Microbiology, 14, 730-742.
Guttenplan, S.B. & Kearns, D.B. (2013) Regulation of flagellar motility during biofilm formation. FEMS Microbiology Reviews, 37, 849-871.
Haiko, J. & Westerlund-Wikstrom, B. (2013) The role of the bacterial flagellum in adhesion and virulence. Biology, 2, 1242-1267.
Harke, M.J., Steffen, M.M., Gobler, C.J., Otten, T.G., Wilhelm, S.W., Wood, S.A. et al. (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae, 54, 4-20.
Herlemann, D.P., Labrenz, M., Jürgens, K., Bertilsson, S., Waniek, J.J. & Andersson, A.F. (2011) Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal, 5, 1571-1579.
Huisman, J., Codd, G.A., Paerl, H.W., Ibelings, B.W., Verspagen, J.M.H. & Visser, P.M. (2018) Cyanobacterial blooms. Nature Reviews Microbiology, 16, 471-483.
Jochim, A., Shi, T., Belikova, D., Schwarz, S., Peschel, A. & Heilbronner, S. (2019) Methionine limitation impairs pathogen expansion and biofilm formation capacity. Applied and Environmental Microbiology, 85, e00177-00119.
Kim, M., Shin, B., Lee, J., Park, H.Y. & Park, W. (2019) Culture-independent and culture-dependent analyses of the bacterial community in the phycosphere of cyanobloom-forming Microcystis aeruginosa. Scientific Reports, 9, 20416.
Li, M., Zhu, W., Gao, L. & Lu, L. (2013) Changes in extracellular polysaccharide content and morphology of Microcystis aeruginosa at different specific growth rates. Journal of Applied Phycology, 25, 1023-1030.
Li, M., Nkrumah, P.N. & Peng, Q. (2015) Different tolerances to chemical contaminants between unicellular and colonial morph of Microcystis aeruginosa: excluding the differences among different strains. Journal of Hazardous Materials, 285, 245-249.
Li, J., Zhang, J., Huang, W., Kong, F., Li, Y., Xi, M. et al. (2016a) Comparative bioavailability of ammonium, nitrate, nitrite and urea to typically harmful cyanobacterium Microcystis aeruginosa. Marine Pollution Bulletin, 110, 93-98.
Li, Z.-K., Dai, G.-Z., Juneau, P. & Qiu, B.-S. (2016b) Capsular polysaccharides facilitate enhanced iron acquisition by the colonial cyanobacterium Microcystis sp isolated from a freshwater lake. Journal of Phycology, 52, 105-115.
Li, Q., Lin, F., Yang, C., Wang, J., Lin, Y., Shen, M. et al. (2018) A large-scale comparative metagenomic study reveals the functional interactions in six bloom-forming Microcystis-epibiont communities. Frontiers in Microbiology, 9, 746.
Lu, K., Liu, Z., Dai, R. & Gardner, W.S. (2019) Urea dynamics during Lake Taihu cyanobacterial blooms in China. Harmful Algae, 84, 233-243.
Madsen, J.S., Burmolle, M., Hansen, L.H. & Sorensen, S.J. (2012) The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunology and Medical Microbiology, 65, 183-195.
Meyer, F., Paarmann, D., D'Souza, M., Olson, R., Glass, E.M., Kubal, M. et al. (2008) The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics, 9, 386.
Plude, J.L., Parker, D.L., Schommer, O.J., Timmerman, R.J., Hagstrom, S.A., Joers, J.M. et al. (1991) Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos-aquae C3-40. Applied and Environmental Microbiology, 57, 1696-1700.
Qin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H.W. et al. (2010) A drinking water crisis in Lake Taihu, China: linkage to climatic variability and lake management. Environmental Management, 45, 105-112.
Robinson, M.D. & Oshlack, A. (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biology, 11, R25.
Sanawar, H., Pinel, I., Farhat, N.M., Bucs, S.S., Zlopasa, J., Kruithof, J.C. et al. (2018) Enhanced biofilm solubilization by urea in reverse osmosis membrane systems. Water Research X, 1, 100004.
Sanders, J.G., Beinart, R.A., Stewart, F.J., Delong, E.F. & Girguis, P.R. (2013) Metatranscriptomics reveal differences in in situ energy and nitrogen metabolism among hydrothermal vent snail symbionts. The ISME Journal, 7, 1556-1567.
Schmittgen, T.D. & Livak, K.J. (2008) Analyzing real-time PCR data by the comparative C(T) method. Nature Protocols, 3, 1101-1108.
Schrevens, S., Van Zeebroeck, G., Riedelberger, M., Tournu, H., Kuchler, K. & Van Dijck, P. (2018) Methionine is required for cAMP-PKA-mediated morphogenesis and virulence of Candida albicans. Molecular Microbiology, 108, 258-275.
Shen, H. & Song, L. (2007) Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia, 592, 475-486.
Shen, H., Niu, Y., Xie, P., Tao, M. & Yang, X. (2011) Morphological and physiological changes in Microcystis aeruginosa as a result of interactions with heterotrophic bacteria. Freshwater Biology, 56, 1065-1080.
Shi, L., Cai, Y., Yang, H., Xing, P., Li, P., Kong, L. et al. (2009a) Phylogenetic diversity and specificity of bacteria associated with Microcystis aeruginosa and other cyanobacteria. Journal of Environmental Sciences (China), 21, 1581-1590.
Shi, L., Cai, Y., Li, P., Yang, H., Liu, Z., Kong, L. et al. (2009b) Molecular identification of the colony-associated cultivable bacteria of the cyanobacterium Microcystis aeruginosa and their effects on algal growth. Journal of Freshwater Ecology, 24, 211-218.
Shi, L., Cai, Y., Wang, X., Li, P., Yu, Y. & Kong, F. (2010) Community structure of bacteria associated with Microcystis colonies from cyanobacterial blooms. Journal of Freshwater Ecology, 25, 193-203.
Shi, L., Cai, Y., Kong, F. & Yu, Y. (2012) Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environmental Microbiology Reports, 4, 669-678.
Smith, D.J., Tan, J.Y., Powers, M.A., Lin, X.N., Davis, T.W. & Dick, G.J. (2021) Individual Microcystis colonies harbour distinct bacterial communities that differ by Microcystis oligotype and with time. Environmental Microbiology, 23, 3020-3036.
Stalder, T. & Top, E. (2016) Plasmid transfer in biofilms: a perspective on limitations and opportunities. npj Biofilms and Microbiomes, 2, 16022.
Straub, C., Quillardet, P., Vergalli, J., de Marsac, N.T. & Humbert, J.F. (2011) A day in the life of microcystis aeruginosa strain PCC 7806 as revealed by a transcriptomic analysis. PLoS One, 6, e16208.
Tillett, D. & Neilan, B.A. (2000) Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. Journal of Phycology, 36, 251-258.
Tomich, M., Planet, P.J. & Figurski, D.H. (2007) The tad locus: postcards from the widespread colonization Island. Nature Reviews Microbiology, 5, 363-375.
Wang, K. & Mou, X. (2021) Coordinated diel gene expression of cyanobacteria and their microbiome. Microorganisms, 9, 1670.
Wang, X., Xie, M., Wu, W., Shi, L., Luo, L. & Li, P. (2013) Differential sensitivity of colonial and unicellular Microcystis strains to an algicidal bacterium Pseudomonas aeruginosa. Journal of Plankton Research, 35, 1172-1176.
Wang, W., Zhang, Y., Shen, H., Xie, P. & Yu, J. (2015) Changes in the bacterial community and extracellular compounds associated with the disaggregation of Microcystis colonies. Biochemical Systematics and Ecology, 61, 62-66.
Wang, W., Shen, H., Shi, P., Chen, J., Ni, L. & Xie, P. (2016) Experimental evidence for the role of heterotrophic bacteria in the formation of Microcystis colonies. Journal of Applied Phycology, 28, 1111-1123.
Wang, D., Xu, A., Elmerich, C. & Ma, L.Z. (2017) Biofilm formation enables free-living nitrogen-fixing rhizobacteria to fix nitrogen under aerobic conditions. The ISME Journal, 11, 1602-1613.
Wang, K., Mou, X., Cao, H., Struewing, I., Allen, J. & Lu, J. (2021) Co-occurring microorganisms regulate the succession of cyanobacterial harmful algal blooms. Environmental Pollution, 288, 117682.
Wilson, A.E., Sarnelle, O. & Tillmanns, A.R. (2006) Effects of cyanobacterial toxicity and morphology on the population growth of freshwater zooplankton: meta-analyses of laboratory experiments. Limnology and Oceanography, 51, 1915-1924.
Wu, X., Wu, Z. & Song, L. (2011) Phenotype and temperature affect the affinity for dissolved inorganic carbon in a cyanobacterium Microcystis. Hydrobiologia, 675, 175-186.
Wu, Q., Zhang, X., Jia, S., Li, J. & Li, P. (2019) Effects of the cultivable bacteria attached to Microcystis colonies on the colony size and growth of Microcystis. Journal of Freshwater Ecology, 34, 663-673.
Xiao, M., Willis, A., Burford, M.A. & Li, M. (2017) Review: a meta-analysis comparing cell-division and cell-adhesion in Microcystis colony formation. Harmful Algae, 67, 85-91.
Xiao, M., Li, M. & Reynolds, C.S. (2018) Colony formation in the cyanobacterium Microcystis. Biological Reviews, 93, 1399-1420.
Xie, M., Ren, M., Yang, C., Yi, H., Li, Z., Li, T. et al. (2016) Metagenomic analysis reveals symbiotic relationship among bacteria in Microcystis-dominated community. Frontiers in Microbiology, 7, 56.
Yang, Z., Kong, F., Shi, X., Zhang, M., Xing, P. & Cao, H. (2008) Changes in the morphology and polysaccharide content of Microcystis aeruginosa (Cyanobacteria) during flagellate grazing. Journal of Phycology, 44, 716-720.
Yang, C., Wang, Q., Simon, P.N., Liu, J., Liu, L., Dai, X. et al. (2017) Distinct network interactions in particle-associated and free-living bacterial communities during a Microcystis aeruginosa bloom in a plateau lake. Frontiers in Microbiology, 8, 1202.
Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S. & Madden, T.L. (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics, 13, 134.
Yu, G.C., Wang, L.G., Han, Y.Y. & He, Q.Y. (2012) clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS, 16, 284-287.
Zatyka, M. & Thomas, C.M. (1998) Control of genes for conjugative transfer of plasmids and other mobile elements. FEMS Microbiology Reviews, 21, 291-319.
Zhang, M., Shi, X., Yu, Y. & Kong, F. (2011) The acclimative changes in photochemistry after colony formation of the cyanobacteria Microcystis aeruginosa. Journal of Phycology, 47, 524-532.
Zhang, P., Chen, M., Zhang, Y., Li, Y., Lu, S. & Li, P. (2018) Autoaggregation and adhesion abilities in bacteria associated with colonies of Microcystis. Hydrobiologia, 823, 205-216.
Zhu, C., Zhang, J., Wang, X., Yang, Y., Chen, N., Lu, Z. et al. (2021) Responses of cyanobacterial aggregate microbial communities to algal blooms. Water Research, 196, 117014.