Abstract
We compared the genetic diversity of the 16S-23S spacer of the rRNA gene (ITS1) in benthic and pelagic colonies of the Microcystis genus isolated from two different sampling stations with different depths and at two different sampling times (winter and summer) in the French storage reservoir of Grangent. In all, 66 ITS1 sequences were found in the different clone libraries. The nucleotide diversity of all the sampled isolates were in the same range (average number = 0.022) regardless of their origin, showing that several clones are involved in the summer bloom event and contribute to the high biomass production. Phylogenetic study and analysis of molecular variance (AMOVA) revealed no obvious genetic differentiation between the benthic and pelagic isolates. This finding confirms that the Microcystis genus in this lake is characterized by having both a benthic phase in winter and spring allowing this organism to survive in unfavorable environmental conditions, and a pelagic phase in summer and autumn when environmental conditions allow them to grow in the water column. Finally, comparing these sequences with those available in the GenBank database showed that some highly conserved genotypes are found throughout the world.
Similar content being viewed by others
References
GLA Barker A Konopka BA Handley PK Hayes (2000) ArticleTitleGenetic variation in Aphanizomenon (Cyanobacteria) colonies from the Baltic Sea and North America J Phycol 36 947–950 Occurrence Handle10.1046/j.1529-8817.2000.99146.x
JL Berthon J Devaux L Aleya H Giraudet F Restituito (1996) ArticleTitleDéterminisme de l’eutrophisation de la retenue de Grangent (Loire): étude des nutriments, de la dynamique des populations phytoplanctoniques et des relations phyto-zooplanctoniques en 1990–1991 Hydroécol Appl 8 99–125
MC Bittencourt-Oliveira M Cabral Oliveira Particlede CJS Bolch (2001) ArticleTitleGenetic variability of Brazilian strains of the Microcystis aeruginosa complex (cyanobacteria/cyanophyceae) using the phycocyanin intergenic spacer and flanking regions (cpcBA) J Phycol 37 810–818 Occurrence Handle10.1046/j.1529-8817.2001.00102.x
RE Blankenship H Hartman (1998) ArticleTitleThe origin and evolution of oxygenic photosynthesis Trends Biochem Sci 23 94–97 Occurrence Handle10.1016/S0968-0004(98)01186-4 Occurrence Handle9581499
AK Brunberg P Blomqvist (2002) ArticleTitleBenthic overwintering of Microcystis colonies under different environmental conditions J Plankton Res 24 1247–1252 Occurrence Handle10.1093/plankt/24.11.1247
AK Brunberg P Blomqvist (2003) ArticleTitleRecruitment of Microcystis (cyanophyceae) from lake sediments: the importance of littoral inocula J Phycol 39 58–63 Occurrence Handle10.1046/j.1529-8817.2003.02059.x
G Christiansen J Fastner M Erhard T Börner E Dittmann (2003) ArticleTitleMicrocystin biosynthesis in Planktothrix: genes, evolution, and manipulation J Bacteriol 185 564–572 Occurrence Handle10.1128/JB.185.2.564-572.2003 Occurrence Handle12511503
L Excoffier PE Smouse JM Quattro (1992) ArticleTitleAnalysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data Genetics 131 479–491 Occurrence Handle1644282
RD Fallon TD Brock (1981) ArticleTitleOverwintering of Microcystis in Lake Mendota Freshwat Biol 11 217–226
J Fastner M Erhard H Döhren Particlevon (2001) ArticleTitleDetermination of oligopeptide diversity within a natural population of Microcystis spp. (Cyanobacteria) by typing single colonies by matrix-assisted laser desorption ionization-time of flight mass spectrometry Appl Environ Microbiol 67 5069–5076 Occurrence Handle10.1128/AEM.67.11.5069-5076.2001 Occurrence Handle11679328
Felsenstein, J (1993) Phylogenetic Inference Programs (PHYLIP), Manual 3.5c. University of Washington, Seattle, Washington. Distributed by the author (http://evolution.genetics.washington.edu/phylip.html)
MJ Ferris M Kuhl A Wieland DM Ward (2003) ArticleTitleCyanobacterial ecotypoes in different optical microenvironments of a 68°C hot spring mat community revealed by 16S-23S rRNA internal transcribed spacer region variation Appl Environ Microbiol 69 2893–2898 Occurrence Handle10.1128/AEM.69.5.2893-2898.2003 Occurrence Handle12732563
BJ Finlay (2002) ArticleTitleGlobal dispersal of free-living microbial eukaryote species Science 296 1061–1063 Occurrence Handle10.1126/science.1070710 Occurrence Handle12004115
M Gugger C Lyra P Henriksen A Couté JF Humbert K Sivonen (2002) ArticleTitlePhylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomenon Int J Syst Evol Microbiol 52 1867–1880 Occurrence Handle10.1099/ijs.0.02270-0 Occurrence Handle12361299
PK Hayes GLA Barker (1997) ArticleTitleGentic diversity within Baltic Sea populations of Nodularia (Cyanobacteria) J Phycol 33 919–923 Occurrence Handle10.1111/j.0022-3646.1997.00919.x
JF Humbert B Le Berre (2001) ArticleTitleGenetic diversity among two freshwater cyanobacteria species, Planktothrix (Oscillatoria) rubescens and P. agardhii Arch Hydrobiol 2 197–206
I Iteman R Rippka N Tandeau Marsac Particlede M Herdman (2000) ArticleTitleComparison of conserved structural and regulatory domains within divergent 16S rRNA–23S rRNA spacer sequences of cyanobacteria Microbiology 146 1275–1286 Occurrence Handle10846207
I Janse M Meima WEA Kardinaal G Zwart (2003) ArticleTitleHigh-resolution differentiation of Cyanobacteria by using rRNA-Internal transcribed spacer denaturing gradient gel electrophoresis Appl Environ Microbiol 69 6634–6643 Occurrence Handle10.1128/AEM.69.11.6634-6643.2003 Occurrence Handle14602623
R Kondo M Komura S Hiroishi Y Hata (1998) ArticleTitleDetection and 16S rDNA sequence analysis of a bloom-forming cyanobacterial genus Microcystis Fish Sci 64 840–841
T Kuiper-Goodman I Falconer J Fitzgerald (1999) Human health aspects I Chorus J Bartram (Eds) Toxic Cyanobacteria in Water E & FN Spon London 113–153
R Kurmayer E Dittmann J Fastner I Chorus (2002) ArticleTitleDiversity of microcystin genes within a population of the toxic Cyanobacterium Microcystis spp. in Lake Wannsee (Berlin, Germany) Microb Ecol 43 107–118 Occurrence Handle10.1007/s00248-001-0039-3 Occurrence Handle11984633
R Kurmayer G Christiansen I Chorus (2003) ArticleTitleThe abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee Appl Environ Micobiol 69 787–795 Occurrence Handle10.1128/AEM.69.2.787-795.2003
MJ Laamanen L Forsström K Sivonen (2002) ArticleTitleDiversity of Aphanizomenon flos-aquae (cyanobacetrium) populations along a Baltic Sea salinity gradient Appl Environ Microbiol 68 5296–5303 Occurrence Handle12406717
Latour, D, Sabido, O, Giraudet, H Use of flow cytometric analysis to assess the metabolic activity and dynamics of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France). J Plankt Res (in revision)
B Mikalsen G Boison OM Skulberg J Fastner W Davies TM Gabrielsen K Rudi KS Jakobsen (2003) ArticleTitleNatural variation in the microcystin synthetase operon mcyABC and impact on microcystin production in Microcystis strains J Bacteriol 185 2774–2785 Occurrence Handle10.1128/JB.185.9.2774-2785.2003 Occurrence Handle12700256
R Moezelaar LJ Stal (1994) ArticleTitleFermentation in the unicellular cyanobacterium Microcystis PCC7806 Arch Microbiol 162 63–69 Occurrence Handle10.1007/s002030050102
LR Moore G Rocap SW Chislholm (1998) ArticleTitlePhysiology and molecular phylogeny of coexisting Prochlorococcus ecotypes Nature 393 464–467 Occurrence Handle10.1038/30965 Occurrence Handle9624000
L Mur (1983) ArticleTitleSome aspects of the ecophysiology of cyanobacteria Ann Microbiol 134 61–72
Nicholas, KB, Nicholas, HB (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author (www.cris.com/∼ketchup/genedoc.shtml)
S Otsuka S Suda R Watanabe H Oyaizu S Matsumoto MM Watanabe (1999) ArticleTitlePhylogenetic relationships between toxic and non-toxic strains of the genus Microcystis based on 16S to 23S internal transcribed spacer sequence FEMS Microbiol Let 172 15–21 Occurrence Handle10.1016/S0378-1097(99)00010-5
S Otsuka S Suda S Shibata H Oyaizu S Matsumoto MM Watanabe (2001) ArticleTitleA proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the bacteriological code Int J Syst Evol Microbiol 51 873–879 Occurrence Handle11411709
Page, RDM (2000) TreeView ver: 1.6.1. Distributed by the author (http://taxonomy.zooiogy.gla.ac.uk/rod/rod.html)
A Rantala DP Fewer M Hisbergues L Rouhiainen J Vaitomaa T Borner K Sivonen (2004) ArticleTitlePhylogenetic evidence for the early evolution of microcystin synthesis Proc Nat Acad Sci USA 101 568–573 Occurrence Handle10.1073/pnas.0304489101 Occurrence Handle14701903
CS Reynolds GHM Jaworski HA Cmiech GF Leedale (1981) ArticleTitleOn the annual cycle of the blue-green alga Microcystis aeruginosa Kutz. Emend. Elenkin Proc R Soc Lond Ser B 293 419–477
Schneider, S, Kueffer, JM, Roessli, D, Excoffier, L (1997) Arlequin ver. 2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland. Distributed by the author (http://lgb.unige.ch/arlequin/)
D Tillet DL Parker BA Neilan (2001) ArticleTitleDetection 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 Appl Environ Microbiol 67 2810–2818 Occurrence Handle10.1128/AEM.67.6.2810-2818.2001 Occurrence Handle11375198
S Tsujimura H Tsukada H Nakahara T Nakajima M Nishino (2000) ArticleTitleSeasonal variations of Microcystis population in the sediments of Lake Biwa, Japan Hydrobiologia 434 183–192 Occurrence Handle10.1023/A:1004077225916
E Urbach SW Chisholm (1998) ArticleTitleGenetic diversity in Prochlorococcus populations flow cytometrically sorted from the Sargossa Sea and Gulf Stream Limnol Oceanogr 43 1615–1630
E Urbach DJ Scanlan DL Distel JB Waterbury SW Chisholm (1998) ArticleTitleRapid diversification of marine picophytoplankton with dissimilar light-harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria) J Mol Evol 46 188–201 Occurrence Handle9452521
G Zwart WD Hiorns BA Methe MP Agterveld Particlevan R Huismans SC Nold JP Zehr HJ Laanbroek (1998) ArticleTitleNearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of globally distributed freshwater bacteria Syst Appl Microbiol 21 546–556 Occurrence Handle9924823
Acknowledgments
We thank S. Gay for technical assistance and M. Gugger for stimulating discussions of the manuscript. The English text has been checked by Monika Ghosh.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Humbert, J., Duris-Latour, D., Berre, B.L. et al. Genetic Diversity in Microcystis Populations of a French Storage Reservoir Assessed by Sequencing of the 16S-23S rRNA Intergenic Spacer. Microb Ecol 49, 308–314 (2005). https://doi.org/10.1007/s00248-004-0004-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-004-0004-z