Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa
1 Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan 2 Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan Correspondence Makoto M. Watanabe makoto{at}bio...
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Published in | Microbiology (Society for General Microbiology) Vol. 153; no. 11; pp. 3695 - 3703 |
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01.11.2007
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Abstract | 1 Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan
2 Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan
Correspondence Makoto M. Watanabe makoto{at}biol.tsukuba.ac.jp
Microcystis aeruginosa is one of the most prevalent bloom-forming cyanobacteria and has been the cause of increasing public health concern due to the production of hepatotoxins (microcystins). To investigate the genetic diversity, clonality and evolutionary genetic background with regard to the toxicity of M. aeruginosa , a multilocus sequence typing (MLST) scheme was developed, based on seven selected housekeeping loci ( ftsZ , glnA , gltX , gyrB , pgi , recA and tpi ). Analysis of a collection of 164 isolates from Japan and other countries identified 79 unique sequence types (STs), revealing a high level of genetic diversity ( H =0.951). Although recombination between loci was indicated to be substantial by Shimodaira–Hasegawa (SH) tests, multilocus linkage disequilibrium analyses indicated that recombination between strains probably occurs at some frequency but not to the extent at which alleles are associated randomly, suggesting that the population structure of M. aeruginosa is clonal. Analysis of subsets of strains also indicated that the clonal population structure is maintained even in a local population. Phylogenetic analysis based on the concatenated sequences of seven MLST loci demonstrated that microcystin-producing genotypes are not monophyletic, providing further evidence for the gain and loss of toxicity during the intraspecific diversification of M. aeruginosa . However, toxic strains are genetically distinct from non-toxic strains in MLST allelic profiles, and it was also shown that non-toxic strains harbouring toxin genes fall into a single monophyletic clade, except for one case. These results suggest that the toxicity of M. aeruginosa is relatively stable in the short term, and therefore can be unequivocally characterized by MLST. The MLST scheme established here will be of great help for future detailed population genetic studies of M. aeruginosa .
Abbreviations: I A , index of association; LC ESI-MS, liquid chromatography electrospray ionization MS; ML, maximum-likelihood; MLST, multilocus sequence typing; NJ, neighbour-joining; NJBP, NJ bootstrap; PP, posterior probability; r D , standardized measure of I A ; SH test, Shimodaira–Hasegawa test; ST, sequence type
The GenBank/EMBL/DDBJ accession numbers for the ftsZ , glnA , gltX , gyrB , pgi , recA and tpi sequences of the Microcystis aeruginosa strains examined in this study are AB324850–AB325402.
A supplementary figure showing the individual phylogenetic trees for the seven MLST loci, and supplementary tables showing strain information and the degenerate primer sequences used for isolating five of the seven MLST genes, are available with the online version of this paper. |
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AbstractList | Microcystis aeruginosa is one of the most prevalent bloom-forming cyanobacteria and has been the cause of increasing public health concern due to the production of hepatotoxins (microcystins). To investigate the genetic diversity, clonality and evolutionary genetic background with regard to the toxicity of M. aeruginosa, a multilocus sequence typing (MLST) scheme was developed, based on seven selected housekeeping loci (ftsZ, glnA, gltX, gyrB, pgi, recA and tpi). Analysis of a collection of 164 isolates from Japan and other countries identified 79 unique sequence types (STs), revealing a high level of genetic diversity (H=0.951). Although recombination between loci was indicated to be substantial by Shimodaira-Hasegawa (SH) tests, multilocus linkage disequilibrium analyses indicated that recombination between strains probably occurs at some frequency but not to the extent at which alleles are associated randomly, suggesting that the population structure of M. aeruginosa is clonal. Analysis of subsets of strains also indicated that the clonal population structure is maintained even in a local population. Phylogenetic analysis based on the concatenated sequences of seven MLST loci demonstrated that microcystin-producing genotypes are not monophyletic, providing further evidence for the gain and loss of toxicity during the intraspecific diversification of M. aeruginosa. However, toxic strains are genetically distinct from non-toxic strains in MLST allelic profiles, and it was also shown that non-toxic strains harbouring toxin genes fall into a single monophyletic clade, except for one case. These results suggest that the toxicity of M. aeruginosa is relatively stable in the short term, and therefore can be unequivocally characterized by MLST. The MLST scheme established here will be of great help for future detailed population genetic studies of M. aeruginosa. 1 Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan 2 Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki 305-8572, Japan Correspondence Makoto M. Watanabe makoto{at}biol.tsukuba.ac.jp Microcystis aeruginosa is one of the most prevalent bloom-forming cyanobacteria and has been the cause of increasing public health concern due to the production of hepatotoxins (microcystins). To investigate the genetic diversity, clonality and evolutionary genetic background with regard to the toxicity of M. aeruginosa , a multilocus sequence typing (MLST) scheme was developed, based on seven selected housekeeping loci ( ftsZ , glnA , gltX , gyrB , pgi , recA and tpi ). Analysis of a collection of 164 isolates from Japan and other countries identified 79 unique sequence types (STs), revealing a high level of genetic diversity ( H =0.951). Although recombination between loci was indicated to be substantial by Shimodaira–Hasegawa (SH) tests, multilocus linkage disequilibrium analyses indicated that recombination between strains probably occurs at some frequency but not to the extent at which alleles are associated randomly, suggesting that the population structure of M. aeruginosa is clonal. Analysis of subsets of strains also indicated that the clonal population structure is maintained even in a local population. Phylogenetic analysis based on the concatenated sequences of seven MLST loci demonstrated that microcystin-producing genotypes are not monophyletic, providing further evidence for the gain and loss of toxicity during the intraspecific diversification of M. aeruginosa . However, toxic strains are genetically distinct from non-toxic strains in MLST allelic profiles, and it was also shown that non-toxic strains harbouring toxin genes fall into a single monophyletic clade, except for one case. These results suggest that the toxicity of M. aeruginosa is relatively stable in the short term, and therefore can be unequivocally characterized by MLST. The MLST scheme established here will be of great help for future detailed population genetic studies of M. aeruginosa . Abbreviations: I A , index of association; LC ESI-MS, liquid chromatography electrospray ionization MS; ML, maximum-likelihood; MLST, multilocus sequence typing; NJ, neighbour-joining; NJBP, NJ bootstrap; PP, posterior probability; r D , standardized measure of I A ; SH test, Shimodaira–Hasegawa test; ST, sequence type The GenBank/EMBL/DDBJ accession numbers for the ftsZ , glnA , gltX , gyrB , pgi , recA and tpi sequences of the Microcystis aeruginosa strains examined in this study are AB324850–AB325402. A supplementary figure showing the individual phylogenetic trees for the seven MLST loci, and supplementary tables showing strain information and the degenerate primer sequences used for isolating five of the seven MLST genes, are available with the online version of this paper. |
Author | Tanabe, Yuuhiko Kasai, Fumie Watanabe, Makoto M |
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Cites_doi | 10.1128/AEM.72.1.117-123.2006 10.1046/j.1365-2958.1997.6131982.x 10.1128/AEM.71.2.629-635.2005 10.1093/oxfordjournals.molbev.a026201 10.1126/science.6999623 10.1016/j.mib.2004.04.002 10.1007/s00203-002-0397-3 10.1128/AEM.61.6.2286-2291.1995 10.1128/AEM.61.11.3875-3883.1995 10.1128/JB.186.8.2355-2365.2004 10.7312/nei-92038 10.1099/00207713-51-3-873 10.1046/j.1471-8278.2000.00014.x 10.2323/jgam.46.39 10.1093/bioinformatics/btg180 10.1093/genetics/123.3.585 10.1073/pnas.0304489101 10.1073/pnas.90.10.4384 10.1128/JCM.40.6.1963-1971.2002 10.1111/j.1574-6968.1999.tb13443.x 10.1099/00221287-146-11-2865 10.1093/oxfordjournals.jbchem.a022481 10.1093/bioinformatics/14.9.817 10.1093/bioinformatics/bth490 10.1002/mnfr.200500162 10.1111/j.1365-294X.1992.tb00161.x 10.1093/bioinformatics/btg359 10.1128/AEM.67.6.2810-2818.2001 10.1099/00221287-144-11-3049 10.1007/s00248-001-0039-3 10.1186/1741-7007-3-6 10.1126/science.1103289 10.1128/AEM.70.7.3979-3987.2004 10.1128/JB.185.9.2774-2785.2003 10.1073/pnas.95.6.3140 10.1016/S1074-5521(00)00021-1 10.1073/pnas.37.3.146 10.1007/s00239-004-2583-1 10.1146/annurev.micro.56.012302.160634 10.1128/AEM.72.2.1239-1247.2006 10.1099/00207713-51-2-513 10.1111/j.1574-6968.1996.tb08564.x 10.1099/00207713-47-3-693 |
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References | Mlouka (R21) 2004; 186 Janse (R14) 2004; 70 Atwood (R2) 1951; 37 Yoshida (R47) 2006; 72 Posada (R31) 1998; 14 Dittmann (R7) 1997; 26 Takahashi (R40) 1996; 145 Istock (R13) 1992; 1 Mikalsen (R20) 2003; 185 Feil (R9) 2004; 7 Kurmayer (R16) 2002; 43 Homan (R12) 2002; 40 Kasai (R15) 2004 Martin (R19) 2005; 21 Wallace (R45) 2002; 177 Papke (R30) 2004; 306 Ronquist (R33) 2003; 19 Otsuka (R27) 1999; 172 Shimodaira (R36) 1999; 16 Tajima (R39) 1989; 123 Lyra (R17) 2001; 51 Swofford (R38) 2002 Maiden (R18) 1998; 95 Smith (R37) 1993; 90 Cohan (R5) 2002; 56 Dittmann (R6) 2006; 50 Christiansen (R4) 2006; 72 Otsuka (R28) 2000; 46 Tillett (R42) 2000; 7 Barker (R3) 2000; 146 Rantala (R32) 2004; 101 Holt (R11) 1994 Hanage (R10) 2005; 3 Neilan (R23) 1995; 61 Rozas (R34) 2003; 19 Watanabe (R46) 1996 Tillett (R43) 2001; 67 Neilan (R25) 1997; 47 Nei (R22) 1987 Tanabe (R41) 2004; 58 Enright (R8) 1998; 144 Neilan (R24) 1995; 61 Otsuka (R29) 2001; 51 Tucker (R44) 2005; 71 Agapow (R1) 2001; 1 Nishizawa (R26) 1999; 126 Selander (R35) 1980; 210 |
References_xml | – volume: 72 start-page: 117 year: 2006 ident: R4 article-title: Transposons inactivate biosynthesis of the nonribosomal peptide microcystin in naturally occurring Planktothrix spp publication-title: Appl Environ Microbiol doi: 10.1128/AEM.72.1.117-123.2006 contributor: fullname: Christiansen – volume-title: NIES-Collection, List of Strains, Microalgae and Protozoa year: 2004 ident: R15 contributor: fullname: Kasai – volume: 26 start-page: 779 year: 1997 ident: R7 article-title: Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806 publication-title: Mol Microbiol doi: 10.1046/j.1365-2958.1997.6131982.x contributor: fullname: Dittmann – volume: 71 start-page: 629 year: 2005 ident: R44 article-title: Identification of cyanophage Ma-LBP and infection of the cyanobacterium Microcystis aeruginosa from an Australian subtropical lake by the virus publication-title: Appl Environ Microbiol doi: 10.1128/AEM.71.2.629-635.2005 contributor: fullname: Tucker – volume: 16 start-page: 1114 year: 1999 ident: R36 article-title: Multiple comparisons of log-likelihoods with applications to phylogenetic inference publication-title: Mol Biol Evol doi: 10.1093/oxfordjournals.molbev.a026201 contributor: fullname: Shimodaira – volume: 210 start-page: 545 year: 1980 ident: R35 article-title: Genetic diversity and structure in Escherichia coli populations publication-title: Science doi: 10.1126/science.6999623 contributor: fullname: Selander – volume: 7 start-page: 308 year: 2004 ident: R9 article-title: Analyses of clonality and the evolution of bacterial pathogens publication-title: Curr Opin Microbiol doi: 10.1016/j.mib.2004.04.002 contributor: fullname: Feil – volume: 177 start-page: 332 year: 2002 ident: R45 article-title: Characterization of pMa025, a plasmid from the cyanobacterium Microcystis aeruginosa UV025 publication-title: Arch Microbiol doi: 10.1007/s00203-002-0397-3 contributor: fullname: Wallace – volume: 61 start-page: 2286 year: 1995 ident: R23 article-title: Identification and phylogenetic analysis of toxigenic Cyanobacteria by multiplex randomly amplified polymorphic DNA PCR publication-title: Appl Environ Microbiol doi: 10.1128/AEM.61.6.2286-2291.1995 contributor: fullname: Neilan – volume: 61 start-page: 3875 year: 1995 ident: R24 article-title: Genetic diversity and phylogeny of toxic cyanobacteria determined by DNA polymorphisms within the phycocyanin locus publication-title: Appl Environ Microbiol doi: 10.1128/AEM.61.11.3875-3883.1995 contributor: fullname: Neilan – volume: 186 start-page: 2355 year: 2004 ident: R21 article-title: The gas vesicle gene cluster from Microcystis aeruginosa and DNA rearrangements that lead to loss of cell buoyancy publication-title: J Bacteriol doi: 10.1128/JB.186.8.2355-2365.2004 contributor: fullname: Mlouka – volume-title: Molecular Evolutionary Genetics year: 1987 ident: R22 doi: 10.7312/nei-92038 contributor: fullname: Nei – volume: 51 start-page: 873 year: 2001 ident: R29 article-title: A proposal for the unification of five species of the cyanobacterial genus Microcystis Kutzing ex Lemmermann 1907 under the rules of the Bacteriological Code publication-title: Int J Syst Evol Microbiol doi: 10.1099/00207713-51-3-873 contributor: fullname: Otsuka – volume: 1 start-page: 101 year: 2001 ident: R1 article-title: Indices of multilocus linkage disequilibrium publication-title: Mol Ecol Notes doi: 10.1046/j.1471-8278.2000.00014.x contributor: fullname: Agapow – volume: 46 start-page: 39 year: 2000 ident: R28 article-title: Morphological variability of colonies of Microcystis morphospecies in culture publication-title: J Gen Appl Microbiol doi: 10.2323/jgam.46.39 contributor: fullname: Otsuka – volume: 19 start-page: 1572 year: 2003 ident: R33 article-title: MrBayes 3: Bayesian phylogenetic inference under mixed models publication-title: Bioinformatics doi: 10.1093/bioinformatics/btg180 contributor: fullname: Ronquist – volume: 123 start-page: 585 year: 1989 ident: R39 article-title: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism publication-title: Genetics doi: 10.1093/genetics/123.3.585 contributor: fullname: Tajima – volume: 101 start-page: 568 year: 2004 ident: R32 article-title: Phylogenetic evidence for the early evolution of microcystin synthesis publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.0304489101 contributor: fullname: Rantala – volume: 90 start-page: 4384 year: 1993 ident: R37 article-title: How clonal are bacteria? publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.90.10.4384 contributor: fullname: Smith – volume: 40 start-page: 1963 year: 2002 ident: R12 article-title: Multilocus sequence typing scheme for Enterococcus faecium publication-title: J Clin Microbiol doi: 10.1128/JCM.40.6.1963-1971.2002 contributor: fullname: Homan – volume: 172 start-page: 15 year: 1999 ident: R27 article-title: Phylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence publication-title: FEMS Microbiol Lett doi: 10.1111/j.1574-6968.1999.tb13443.x contributor: fullname: Otsuka – volume: 146 start-page: 2865 year: 2000 ident: R3 article-title: Allele-specific PCR shows that genetic exchange occurs among genetically diverse Nodularia (cyanobacteria) filaments in the Baltic Sea publication-title: Microbiology doi: 10.1099/00221287-146-11-2865 contributor: fullname: Barker – volume: 126 start-page: 520 year: 1999 ident: R26 article-title: Genetic analysis of the peptide synthetase genes for a cyclic heptapeptide microcystin in Microcystis spp publication-title: J Biochem (Tokyo ) doi: 10.1093/oxfordjournals.jbchem.a022481 contributor: fullname: Nishizawa – volume: 14 start-page: 817 year: 1998 ident: R31 article-title: MODELTEST: testing the model of DNA substitution publication-title: Bioinformatics doi: 10.1093/bioinformatics/14.9.817 contributor: fullname: Posada – volume: 21 start-page: 260 year: 2005 ident: R19 article-title: RDP2: recombination detection and analysis from sequence alignments publication-title: Bioinformatics doi: 10.1093/bioinformatics/bth490 contributor: fullname: Martin – volume: 50 start-page: 7 year: 2006 ident: R6 article-title: Cyanobacterial toxins – occurrence, biosynthesis and impact on human affairs publication-title: Mol Nutr Food Res doi: 10.1002/mnfr.200500162 contributor: fullname: Dittmann – volume: 1 start-page: 95 year: 1992 ident: R13 article-title: Sexuality in a natural population of bacteria – Bacillus subtilis challenges the clonal paradigm publication-title: Mol Ecol doi: 10.1111/j.1365-294X.1992.tb00161.x contributor: fullname: Istock – volume: 19 start-page: 2496 year: 2003 ident: R34 article-title: DnaSP, DNA polymorphism analyses by the coalescent and other methods publication-title: Bioinformatics doi: 10.1093/bioinformatics/btg359 contributor: fullname: Rozas – volume: 67 start-page: 2810 year: 2001 ident: R43 article-title: Detection of toxigenicity by a probe for the microcystin synthetase A gene ( mcyA) of the cyanobacterial genus Microcystis: comparison of toxicities with 16S rRNA and phycocyanin operon (phycocyanin intergenic spacer) phylogenies publication-title: Appl Environ Microbiol doi: 10.1128/AEM.67.6.2810-2818.2001 contributor: fullname: Tillett – volume: 144 start-page: 3049 year: 1998 ident: R8 article-title: A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease publication-title: Microbiology doi: 10.1099/00221287-144-11-3049 contributor: fullname: Enright – volume: 43 start-page: 107 year: 2002 ident: R16 article-title: Diversity of microcystin genes within a population of the toxic cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany) publication-title: Microb Ecol doi: 10.1007/s00248-001-0039-3 contributor: fullname: Kurmayer – volume: 3 start-page: 6 year: 2005 ident: R10 article-title: Fuzzy species among recombinogenic bacteria publication-title: BMC Biol doi: 10.1186/1741-7007-3-6 contributor: fullname: Hanage – volume: 306 start-page: 1928 year: 2004 ident: R30 article-title: Frequent recombination in a saltern population of Halorubrum publication-title: Science doi: 10.1126/science.1103289 contributor: fullname: Papke – volume: 70 start-page: 3979 year: 2004 ident: R14 article-title: Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity publication-title: Appl Environ Microbiol doi: 10.1128/AEM.70.7.3979-3987.2004 contributor: fullname: Janse – volume-title: paup* – Phylogenetic analysis using parsimony (*and other methods), version 4 year: 2002 ident: R38 contributor: fullname: Swofford – volume: 185 start-page: 2774 year: 2003 ident: R20 article-title: Natural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains publication-title: J Bacteriol doi: 10.1128/JB.185.9.2774-2785.2003 contributor: fullname: Mikalsen – volume: 95 start-page: 3140 year: 1998 ident: R18 article-title: Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.95.6.3140 contributor: fullname: Maiden – volume: 7 start-page: 753 year: 2000 ident: R42 article-title: Structural organization of microcystin biosynthesis in Microcystis aeruginosa PCC7806: an integrated peptide-polyketide synthetase system publication-title: Chem Biol doi: 10.1016/S1074-5521(00)00021-1 contributor: fullname: Tillett – volume: 37 start-page: 146 year: 1951 ident: R2 article-title: Periodic selection in Escherichia coli publication-title: Proc Natl Acad Sci U S A doi: 10.1073/pnas.37.3.146 contributor: fullname: Atwood – start-page: 377 volume-title: In Bergey's Manual of Determinative Bacteriology year: 1994 ident: R11 article-title: Group 11. Oxygenic phototrophic bacteria contributor: fullname: Holt – volume: 58 start-page: 633 year: 2004 ident: R41 article-title: Evidence for recombination in the microcystin synthetase ( mcy) genes of toxic cyanobacteria Microcystis spp publication-title: J Mol Evol doi: 10.1007/s00239-004-2583-1 contributor: fullname: Tanabe – volume: 56 start-page: 457 year: 2002 ident: R5 article-title: What are bacterial species? publication-title: Annu Rev Microbiol doi: 10.1146/annurev.micro.56.012302.160634 contributor: fullname: Cohan – volume: 72 start-page: 1239 year: 2006 ident: R47 article-title: Isolation and characterization of a cyanophage infecting the toxic cyanobacterium Microcystis aeruginosa publication-title: Appl Environ Microbiol doi: 10.1128/AEM.72.2.1239-1247.2006 contributor: fullname: Yoshida – volume: 51 start-page: 513 year: 2001 ident: R17 article-title: Molecular characterization of planktic cyanobacteria of Anabaena, Aphanizomenon, Microcystis and Planktothrix genera publication-title: Int J Syst Evol Microbiol doi: 10.1099/00207713-51-2-513 contributor: fullname: Lyra – volume: 145 start-page: 107 year: 1996 ident: R40 article-title: Restriction barrier composed of an extracellular nuclease and restriction endonuclease in the unicellular cyanobacterium Microcystis sp publication-title: FEMS Microbiol Lett doi: 10.1111/j.1574-6968.1996.tb08564.x contributor: fullname: Takahashi – volume: 47 start-page: 693 year: 1997 ident: R25 article-title: rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis publication-title: Int J Syst Bacteriol doi: 10.1099/00207713-47-3-693 contributor: fullname: Neilan – start-page: 13 volume-title: In Toxic Microcystis year: 1996 ident: R46 article-title: Isolation, cultivation, and classification of bloom-forming Microcystis in Japan contributor: fullname: Watanabe |
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Snippet | 1 Environmental Biology Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan
2 Graduate School of Life and... Microcystis aeruginosa is one of the most prevalent bloom-forming cyanobacteria and has been the cause of increasing public health concern due to the... |
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SubjectTerms | Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Toxins - genetics Bacterial Toxins - toxicity Bacterial Typing Techniques Bacteriology Biological and medical sciences Cyanobacteria Cyanophyta Evolution, Molecular Fundamental and applied biological sciences. Psychology Genes. Genome Genetic Variation Genetics Genetics, Population Linkage Disequilibrium Microbiology Microcystins - genetics Microcystins - toxicity Microcystis - classification Microcystis - genetics Microcystis aeruginosa Molecular and cellular biology Molecular genetics Molecular Sequence Data Phylogeny Recombination, Genetic Sequence Analysis, DNA |
Title | Multilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosa |
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