Genetic variability of the invasive cyanobacteria Cylindrospermopsis raciborskii from Bir M'cherga reservoir (Tunisia)

Archives of Microbiology

Volumn 193, Issue 8, 2011, Pages 595-604

  Fathalli, Afef ^a   Jenhani, Amel Ben Rejeb ^a   Moreira, Cristiana ^b   Azevedo, Joana ^b   Welker, Martin ^c,d   Romdhane, Mohamed ^a   Antunes, Agostinho ^b   Vasconcelos, Vitor ^b,e  

^a INSTITUT NATIONAL AGRONOMIQUE DE TUNISIE   (Tunisia)

^b UNIVERSITY OF PORTO   (Portugal)

^c AnagnosTec Gesellschaft fur Analytische Biochemie & Diagnostik mbH   (Germany)

^d TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

^e UNIVERSITY OF PORTO   (Portugal)

Author keywords

Cylindrospermopsis raciborskii; mcyA and mcyE; Phylogenetic analysis; Toxicity; Tunisia

Indexed keywords

CYLINDROSPERMOPSIN; MICROCYSTIN; MICROCYSTIN SYNTHETASE; RNA 16S; SAXITOXIN; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII; GENE CLUSTER; GENETIC VARIABILITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MCYA GENE; MCYE GENE; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; RNA SEQUENCE; RPOC1 GENE; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE; TUNISIA; WATER SUPPLY;

CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYLINDROSPERMOPSIS; DNA, BACTERIAL; FRESH WATER; GENETIC VARIATION; MICROCYSTINS; MULTIGENE FAMILY; PHYLOGENY; RNA, RIBOSOMAL, 16S; SAXITOXIN; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TUNISIA; URACIL; WATER MICROBIOLOGY; WATER SUPPLY;

CYANOBACTERIA; CYLINDROSPERMOPSIS RACIBORSKII;

EID: 79960897396     PISSN: 03028933     EISSN: 1432072X     Source Type: Journal    
DOI: 10.1007/s00203-011-0704-y     Document Type: Article

References (64)

1. M Aboal M-A Puig 2005 Intracellular and dissolved microcystin in reservoirs of the river Segura basin, Murcia, SE Spain Toxicon 45 509 518 15733573 10.1016/j.toxicon.2004.12.012 1:CAS:528:DC%2BD2MXhs1Ghurw%3D (Pubitemid 40269941)
2. A Alster RN Kaplan-Levy A Sukenik T Zohary 2010 Morphology and phylogeny of a non-toxic invasive Cylindrospermopsis raciborskii from a Mediterranean Lake Hydrobiologia 639 115 128 10.1007/s10750-009-0044-y
3. C Bernard M Harvey JF Briand R Bire S Krys JJ Fontaine 2003 Toxicological comparison of diverse Cylindrospermopsis raciborskii strains, evidence of liver damage caused by a French C. raciborskii strain Environ Toxicol 18 176 186 12740803 10.1002/tox.10112 1:CAS:528:DC%2BD3sXksFentrc%3D (Pubitemid 36790038)
4. N Bouaïcha AB Nasri 2004 First report of cyanobacterium Cylindrospermopsis raciborskii from Algerian freshwaters Environ Toxicol 19 541 543 15352271 10.1002/tox.20058 (Pubitemid 39419633)
5. ATC Bourke RB Hawes A Neilson ND Stallman 1983 An outbreak of the hepatoenteritis (the Palm Island mystery disease) possibly caused by algal intoxication Toxicon 3 45 48 10.1016/0041-0101(83)90151-4
6. JF Briand S Jacquet C Bernard JF Humbert 2003 Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water ecosystems Vet Res 34 361 377 12911854 10.1051/vetres:2003019 1:CAS:528:DC%2BD3sXnvFyhsbk%3D (Pubitemid 37121280)
7. WW Carmichael 1994 The toxins of cyanobacteria Sci Am 270 78 86 8284661 10.1038/scientificamerican0194-78 1:CAS:528:DyaK2cXkslCnuw%3D%3D
8. AD Chapman CL Schelske 1997 Recent appearance of Cylindrospermopsis (Cyanobacteria) in five hypereutrophic Florida lakes J Phycol 33 191 195 10.1111/j.0022-3646.1997.00191.x
9. D Chonudomkul W Yongmanitchai G Threeragool M Kawachi F Kasai K Kaya MM Watanabe 2004 Morphology, genetic diversity, temperature tolerance and toxicity of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) strains from Thailand and Japan FEMS Microbiol Ecol 48 345 355 19712304 10.1016/j.femsec. 2004.02.014 1:CAS:528:DC%2BD2cXktF2kuro%3D (Pubitemid 38648922)
10. JC Druart JF Briand 2002 First record of Cylindrospermopsis raciborskii (Woloszyn - ska) Seenayya et Subba Raju (Cyanobacteria) in a lotic system in France Ann Limnol Int J Lim 38 339 342 10.1051/limn/2002028
11. J Dyble HW Paerl BA Neilan 2002 Genetic characterization of Cylindrospermopsis raciborskii (cyanobacteria) isolates from diverse geographic origins based on nifH and pcBA-IGS nucleotide sequence analysis Appl Environ Microbiol 68 2567 2571 11976136 10.1128/AEM.68.5.2567-2571.2002 1:CAS:528:DC%2BD38XjsFGqurk%3D (Pubitemid 34477859)
12. J Fastner M Erhard H Von-Döhren 2001 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 11679328 10.1128/AEM.67.11. 5069-5076.2001 1:CAS:528:DC%2BD3MXotlSgu7g%3D (Pubitemid 33701272)
13. J Fastner R Heinze AR Humpage U Mischke GK Eaglesham I Chorus 2003 Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (Cyanobacteria) isolates Toxicon 42 313 321 14559084 10.1016/S0041-0101(03)00150-8 1:CAS:528:DC%2BD3sXnvFGmtb4%3D (Pubitemid 37338169)
14. A Fathalli A Jenhani M Saker C Moreira MS Romdhane VM Vasconcelos 2010 First observation of the toxic and invasive cyanobacterium species Cylindrospermopsis raciborskii in Tunisian freshwaters. Toxicity assessment and molecular characterization Fresenius Environ Bull 19 1074 1083 1:CAS:528:DC%2BC3cXotlagur0%3D
15. KM Fergusson CP Saint 2003 Multiplex PCR Assay for Cylindrospermopsis raciborskii and cylindrospermopsin-producing cyanobacteria Environ Toxicol 18 120 125 12635100 10.1002/tox.10108 1:CAS:528:DC%2BD3sXivVeksrc%3D (Pubitemid 44783329)
16. Garcia C (2001) Isolamento e toxicologia de estirpes de Microcystis aeruginosa da Lagoa de Mira. MSc Thesis, Faculty of Sciences, Porto University
17. M Gugger R Molica B Le Berre P Dufour C Bernard JF Humbert 2005 Genetic diversity of Cylindrospermopsis strains (Cyanobacteria) isolated from four continents Appl Environ Microbiol 71 1097 1100 15691973 10.1128/AEM.71.2.1097- 1100.2005 1:CAS:528:DC%2BD2MXhsVKgtb8%3D (Pubitemid 40223602)
18. S Haande T Rohrlack A Ballot K Røberg R Skulberg M Beck C Wiedner 2008 Genetic characterisation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) isolates from Africa and Europe Harmful Algae 7 692 701 10.1016/j.hal.2008.02.010 1:CAS:528:DC%2BD1cXovFemtLw%3D
19. PB Hamilton LM Ley S Dean FR Pick 2005 The occurrence of the cyanobacterium Cylindrospermopsis raciborskii in Constance Lake, an exotic cyanoprokaryote new to Canada Phycologia 44 17 25 10.2216/0031-8884(2005)44[17: TOOTCC]2.0.CO;2 (Pubitemid 40274197)
20. PR Hawkins MTC Runnegar ARB Jackson IR Falconer 1985 Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green algae) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir Appl Environ Microbiol 50 1292 1295 3937492 1:STN:280:DyaL287ivFejtg%3D%3D (Pubitemid 16193446)
21. PR Hawkins NR Chandrasena GJ Jones AR Humpage IR Falconer 1997 Isolation and toxicity of Cylindrospermopsis raciborskii from an ornamental lake Toxicon 35 341 346 9080590 10.1016/S0041-0101(96)00185-7 1:CAS:528:DyaK2sXhsl2msb8%3D (Pubitemid 27102255)
22. M Hisbergues G Christiansen L Rouhiainen K Sivonen T Börner 2003 PCR-based identification of microcystin-producing genotypes of different cyanobacterial genera Arch Microbiol 180 402 410 14551674 10.1007/s00203-003- 0605-9 1:CAS:528:DC%2BD3sXpsVOisLc%3D (Pubitemid 38002308)
23. Y Hong A Steinman B Biddanda R Rediske G Fahnenstiel 2006 Occurrence of the Toxin-producing Cyanobacterium Cylindrospermopsis raciborskii in Mona and Muskegon Lakes, Michigan J Great Lakes Res 32 645 652 10.3394/0380-1330(2006) 32[645:OOTTCC]2.0.CO;2 (Pubitemid 44619274)
24. V Istvanovics HM Shafik M Presing S Juhos 2000 Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in through flow cultures Freshwater Biol 43 257 275 10.1046/j.1365-2427.2000.00549.x (Pubitemid 30079136)
25. G Izaguirre AD Jungblut BA Neilan 2007 Benthic cyanobacteria (Oscillatoriacea) that produce microcystin-LR, isolated from four reservoirs in Southern California Water Res 41 492 498 17126876 10.1016/j.watres.2006.10.012 1:CAS:528:DC%2BD28XhtlCmt7vN (Pubitemid 44940896)
26. S Janse van Vuuren GP Kriel 2008 Cylindrospermopsis raciborskii, a toxic invasive cyanobacterium in South African freshwaters Afr J Aquat Sci 33 17 26 10.2989/AJAS.2007.33.1.2.386 (Pubitemid 351913809)
27. A-D Jungblut BA Neilan 2006 Molecular identification and evolution of the cyclic peptide hepatotoxins, microcystin and nodularin, synthetase genes in three orders of cyanobacteria Arch Microbiol 185 107 114 16402223 10.1007/s00203-005-0073-5 1:CAS:528:DC%2BD28Xht1ClsL0%3D (Pubitemid 43221204)
28. R Kellmann T Mills BA Neilan 2006 Functional modeling and phylogenetic distribution of putative cylindrospermopsin biosynthesis enzymes J Mol Evol 62 267 280 16508696 10.1007/s00239-005-0030-6 1:CAS:528:DC%2BD28XitlKgsLs%3D
29. R Kellmann TK Mihali YJ Jeon R Pickford F Pomati BA Neilan 2008 Biosynthetic intermediate analysis and functional homology reveal a saxitoxin gene cluster in cyanobacteria Appl Environ Microbiol 74 4044 4053 18487408 10.1128/AEM.00353-08 1:CAS:528:DC%2BD1cXot1Omsb8%3D (Pubitemid 351962430)
30. N Lagos H Onodera PA Zagatto D Andrinolo SMFO Azevedo Y Oshima 1999 The first evidence of paralytic shellfish toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil Toxicon 37 1359 1373 10414862 10.1016/S0041-0101(99)00080-X 1:CAS:528:DyaK1MXktVOqtLY%3D (Pubitemid 29264099)
31. R Li WW Carmichael S Brittain GK Eaglesham GR Shaw A Mahakhant N Noparatnaraporn W Yongmanitchai K Kaya MM Watanabe 2001 Isolation and identification of the cyanotoxin cylindrospermopsin and deoxy-cylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria) Toxicon 39 973 980 11223086 10.1016/S0041-0101(00)00236-1 1:CAS:528: DC%2BD3MXit1ars74%3D (Pubitemid 32166947)
32. G Manti D Mattei V Messineo S Melchiorre S Bogialli N Sechi P Casiddu L Luglié M Di Brizio M Bruno 2005 First report of Cylindrospermopsis raciborskii in Italy Harmful Algal News 28 8 9
33. V Messineo S Melchiorre A Di Corcia P Gallo M Bruno 2010 Seasonal succession of Cylindrospermopsis raciborskii and Aphanizomenon ovalisporum Blooms with Cylindrospermopsin occurrence in the Volcanic Lake Albano, Central Italy Environ Toxicol 25 18 27 19161233 1:CAS:528:DC%2BC3cXhslWrsLk%3D
34. TK Mihali R Kellmann J Muenchhoff KD Barrow BA Neilan 2008 Characterization of the gene cluster responsible for cylindrospermopsin biosynthesis Appl Environ Microbiol 74 716 722 18065631 10.1128/AEM.01988-07 1:CAS:528:DC%2BD1cXhvVSqu7o%3D (Pubitemid 351225723)
35. ZA Mohamed 2007 First report of toxic Cylindrospermopsis raciborskii and Raphidiopsis mediterranea (Cyanoprokaryota) in Egyptian fresh waters FEMS Microbiol Ecol 59 749 761 17069621 10.1111/j.1574-6941.2006.00226.x 1:CAS:528:DC%2BD2sXjsV2jsrs%3D (Pubitemid 46376231)
36. D Moore M O'Donohue C Garnett C Critchley G Shaw 2005 Factors affecting akinete differentiation in Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) Freshwater Biol 50 345 352 10.1111/j.1365-2427.2004.01324.x (Pubitemid 40210704)
37. M Moustaka-Gouni E Vardaka E Tryfon 2007 Phytoplankton species succession in a shallow Mediterranean lake (L. Kastoria, Greece): steady-state dominance of Limnothrix redekei, Microcystis aeruginosa and Cylindrospermopsis raciborskii Hydrobiologia 575 129 140 10.1007/s10750-006-0360-4 (Pubitemid 44900419)
38. BA Neilan D Jacobs T DelDot LL Blackall PR Hawkins PT Cox AE Goodman 1997 rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis Int J Syst Bacteriol 47 693 697 9226902 10.1099/00207713-47-3-693 1:CAS:528:DyaK2sXkvFChtLk%3D (Pubitemid 27327757)
39. BA Neilan ML Saker J Fastner A Törökna BP Burns 2003 Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii Mol Ecol 12 133 140 12492883 10.1046/j.1365-294X.2003.01709.x 1:CAS:528: DC%2BD3sXht1Sjtbs%3D (Pubitemid 36108112)
40. D Nonneman PV Zimba 2002 A PCR-based test to assess the potential for microcystin occurrence in channel catfish production ponds J Phycol 38 230 233 10.1046/j.1529-8817.2002.01138.x (Pubitemid 34196843)
41. O.C.D.E. (1982) Eutrophisation des eaux, méthodes de surveillance, d'évaluation et de lutte. O.C.D.E., Paris, 165p
42. I Ohtani RE Moore MTC Runnegar 1992 Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii J Am Chem Soc 114 7941 7942 10.1021/ja00046a067 1:CAS:528:DyaK38XlvVOqs7Y%3D
43. Y Ouahid GF Pérez-Silva F del Campo 2005 Identification of potentially toxic environmental Microcystis by individual and multiple PCR amplification of specific microcystin synthetase gene regions Environ Toxicol 20 235 242 15892074 10.1002/tox.20103 1:CAS:528:DC%2BD2MXlvFGjtLk%3D (Pubitemid 40827440)
44. J Padisák 1997 Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding highly adaptive blue-green algal species, worldwide distribution and review of its ecology Arch Hydrobiol 107 Suppl 563 593
45. Padisák J (1998) Sudden and gradual responses of phytoplankton to global climate change: case studies from two large, shallow lakes (Balaton, Hungary, and the Neusiedlersee, Austria/Hungary). In: George DG, Jones JG, Puncochar P, Reynolds CS, Sutcliffe DW (eds) Management of lakes and reservoirs during global change. Kluwer Academic Publishers, London, pp 111-125
46. K Preuel A Stüken C Wiedner I Chorus J Fastner 2006 First report on cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) isolated from two German lakes Toxicon 47 156 162 16356522 10.1016/j.toxicon.2005.10.013 (Pubitemid 43143224)
47. Ressom R, Soong FS, Fitzgerald J, Turczynowicz L, Saadi OE, Roder D, Maynard T, Falconer IR (1994) Health effects of toxic cyanobacteria (Blue-Green Algae). National Health and Medical Research Council. Australian Government Publishing Service, Canberra
48. R Rippka J Deruelles JB Waterbury M Herdman RY Stanier 1979 Generic assignments, strain histories and properties of pure cultures of cyanobacteria J Gen Microbiol 111 1 61 (Pubitemid 9142236)
49. S Romo MR Miracle 1994 Population dynamics and ecology of subdominant phytoplankton species in a shallow hypertrophic lake (Albufera of Valencia, Spain) Hydrobiologia 273 37 56 10.1007/BF00126767 (Pubitemid 2043947)
50. J Rücker C Wiedner P Zippel 1997 Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekeii in eutrophic shallow lakes Hydrobiologia 342 107 115 10.1023/A:1017013208039 (Pubitemid 27331513)
51. Saker ML (2000) Cyanobacterial blooms in tropical north Queensland water bodies. PhD Thesis, James Cook University, Townsville, Australia
52. ML Saker GK Eaglesham 1999 The accumulation of cylindrospermopsin from the cyanobacterium Cylindrospermopsis raciborskii in tissues of the Redclaw crayfish Cherax quadricarinatus Toxicon 37 1065 1077 10484741 10.1016/S0041-0101(98)00240-2 1:CAS:528:DyaK1MXjslCrtLw%3D (Pubitemid 29234095)
53. ML Saker BA Neilan 2001 Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from northern Australia Appl Environ Microbiol 67 1839 1845 11282641 10.1128/AEM.67.4.1839-1845.2001 1:CAS:528: DC%2BD3MXis1egtb0%3D (Pubitemid 33644958)
54. ML Saker AD Thomas JH Norton 1999 Cattle mortality attributed to the toxic cyanobacterium Cylindrospermopsis raciborskii in an outback region of north Queensland Environ Toxicol 14 179 183 10.1002/(SICI)1522-7278(199902)14: 1<179::AID-TOX23>3.0.CO;2-G 1:CAS:528:DyaK1MXntl2jtw%3D%3D
55. ML Saker ICG Nogueira VM Vasconcelos BA Neilan GK Eaglesham P Pereira 2003 First report and toxicological assessment of the cyanobacterium Cylindrospermopsis raciborskii from Portuguese freshwaters Ecotoxicol Environ Saf 55 243 250 12742375 10.1016/S0147-6513(02)00043-X 1:CAS:528: DC%2BD3sXjs1eqsbo%3D (Pubitemid 36555411)
56. MA Schembri BA Neilan CP Saint 2001 Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii Environ Toxicol 16 413 421 11594028 10.1002/tox.1051 1:CAS:528:DC%2BD3MXnt1Crsbk%3D (Pubitemid 33040532)
57. G Shalev-Alon A Sukenik O Livnah R Schwarz A Kaplan 2002 A novel gene encoding amidinotransferase in the cylindrospermopsin producing cyanobacterium Aphanizomenon ovalisporum FEMS Microbiol Lett 209 87 91 12007659 10.1111/j.1574-6968.2002.tb11114.x 1:CAS:528:DC%2BD38Xjtl2gsr4%3D (Pubitemid 34457987)
58. Tamura D, Nei K (2007) Phylogenetic and molecular evolutionary analyses were conducted using MEGA version 4
59. E Vardaka M Moustaka-Gouni CM Cook T Lanaras 2005 Cyanobacterial blooms and water quality in Greek waterbodies J Appl Phys 17 391 401 (Pubitemid 41483272)
60. ZZ Varkonyi O Farkas T Garab Z Gombos 2000 The tolerance of cyanobacterium Cylindrospermopsis raciborskii to low-temperature photo-inhibition affected by the induction of polyunsaturated fatty-acid synthesis Biochem Soc T 28 892 894 10.1042/BST0280892 1:CAS:528: DC%2BD3MXhsVGqtbg%3D (Pubitemid 32163307)
61. V Vasconcelos 2006 Eutrophication, toxic cyanobacteria and cyanotoxins: when ecosystems cry for help Limnetica 25 425 432 (Pubitemid 44211112)
62. M Welker H Bickel J Fastner 2002 HPLC-PDA detection of cylindrospermopsin opportunities and limits Water Res 36 4659 4663 12418670 10.1016/S0043-1354(02) 00194-X 1:CAS:528:DC%2BD38XmvF2ktbg%3D (Pubitemid 35286852)
63. KM Wilson MA Schembri PD Baker CP Saint 2000 Molecular characterisation of the toxic cyanobacterium Cylindrospermopsis raciborskii and design of a species-specific PCR Appl Environ Microbiol 66 332 338 10618244 10.1128/AEM.66.1.332-338.2000 1:CAS:528:DC%2BD3cXktlSkug%3D%3D (Pubitemid 30030536)
64. SA Wood DJ Stirling 2003 First identification of the cylindrospermopsin producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand New Zealand J Mar Freshw Res 37 821 828 10.1080/00288330.2003.9517211 1:CAS:528:DC%2BD2cXmt1CnsA%3D%3D (Pubitemid 38065633)