Occurrence of non-cylindrospermopsin-producing Aphanizomenon ovalisporum and Anabaena bergii in Lake Kinneret (Israel)

Ballot, Andreas; Ramm, Jessica; Rundberget, Thomas; Kaplan-Levy, Ruth N.; Hadas, Ora; Sukenik, Assaf; Wiedner, Claudia

doi:10.1093/plankt/fbr071

Cited by 50 publications

(36 citation statements)

References 40 publications

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“…Our results are in accord with those demonstrating the presence of cyr genes in several non-CYN-producing Anabaena bergii and Aphanizomenon ovalisporum strains (29) and in ATX-producing A. issatschenkoi CAWBG02 (24) and of the small cyr-like gene fragment (orf2) in PSP toxin-producing Lyngbya wollei (62). These findings, together with the lack of phylogenetic separation between toxic and nontoxic strains (9,19,29; the present study), suggest a complex evolutionary history of horizontal gene transfer and events of insertions, deletions, and recombination that have shaped toxin biosynthesis genes in cyanobacteria (24,67); such a complex evolutionary history represents one of the emerging challenges for microbiological research.…”

Section: Discussionsupporting

confidence: 91%

“…Studies have shown levels of 9.4 to 18 g CYN liter Ϫ1 during A. ovalisporum blooms in Spain and Italy (57,58). A. ovalisporum is characterized by its genetic homogeneity worldwide (9; this study) and an unusually high proportion of CYN-producing strains, although 2 non-CYN-producing strains have recently been reported from Lake Kinneret, Israel (29). CYN contents seem to vary slightly among strains (e.g., Accession numbers are given in parentheses (strains from GenBank) or listed in Table S1 in the supplemental material (strains from this study).…”

Section: Discussionmentioning

confidence: 66%

“…Methods are also available for the amplification of the sxtA gene, a polyketide synthase involved in the first steps of STX biosynthesis in Anabaena, Anabaenopsis, and Aphanizomenon strains (19). Overall, the studies have shown the strain-specific nature of toxin production, as illustrated by the non-CYN-producing Anabaena bergii and A. ovalisporum strains that contain the cyrA, cyrB, and cyrC genes (29) but lack the cyrJ gene, which is present only in CYN-producing strains (22,29). Interestingly, the separation between toxin-producing and non-toxin-producing strains is linked to biogeographic patterns in certain Nostocales, such as C. raciborskii, with CYN-producing strains occurring in Australia and Asia but non-CYN-producing strains occurring in Africa, Europe, and North America (30) and PSP toxin-producing strains occurring in Brazil and Uruguay (15,31).…”

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confidence: 99%

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Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Cirés

Wörmer

Ballot

et al. 2014

Appl Environ Microbiol

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dPlanktonic Nostocales cyanobacteria represent a challenge for microbiological research because of the wide range of cyanotoxins that they synthesize and their invasive behavior, which is presumably enhanced by global warming. To gain insight into the phylogeography of potentially toxic Nostocales from Mediterranean Europe, 31 strains of Anabaena (Anabaena crassa, A. lemmermannii, A. mendotae, and A. planctonica), Aphanizomenon (Aphanizomenon gracile, A. ovalisporum), and Cylindrospermopsis raciborskii were isolated from 14 freshwater bodies in Spain and polyphasically analyzed for their phylogeography, cyanotoxin production, and the presence of cyanotoxin biosynthesis genes. The potent cytotoxin cylindrospermopsin (CYN) was produced by all 6 Aphanizomenon ovalisporum strains at high levels (5.7 to 9.1 g CYN mg ؊1 [dry weight]) with low variation between strains (1.5 to 3.9-fold) and a marked extracellular release (19 to 41% dissolved CYN) during exponential growth. Paralytic shellfish poisoning (PSP) neurotoxins (saxitoxin, neosaxitoxin, and decarbamoylsaxitoxin) were detected in 2 Aphanizomenon gracile strains, both containing the sxtA gene. This gene was also amplified in non-PSP toxin-producing Aphanizomenon gracile and Aphanizomenon ovalisporum. Phylogenetic analyses supported the species identification and confirmed the high similarity of Spanish Anabaena and Aphanizomenon strains with other European strains. In contrast, Cylindrospermopsis raciborskii from Spain grouped together with American strains and was clearly separate from the rest of the European strains, raising questions about the current assumptions of the phylogeography and spreading routes of C. raciborskii. The present study confirms that the nostocalean genus Aphanizomenon is a major source of CYN and PSP toxins in Europe and demonstrates the presence of the sxtA gene in CYN-producing Aphanizomenon ovalisporum.

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Section: Discussionsupporting

confidence: 91%

Section: Discussionmentioning

confidence: 66%

mentioning

confidence: 99%

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Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Cirés

Wörmer

Ballot

et al. 2014

Appl Environ Microbiol

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“…It seems to be worldwide distributed, having been detected amongst other regions in Australia, Europe, Middle East and United States [4]. In the last decades, the presence of A. ovalisporum has become an important health hazard, because all strains found, with only one exception in Israel [5], produce the toxic alkaloid cylindrospermopsin (CYN).…”

Section: Introductionmentioning

confidence: 99%

Dynamics of Cylindrospermopsin Production and Toxin Gene Expression in <i>Aphanizomenon ovalisporum</i>

Barón‐Solá¹,

Campo²,

Sanz-Alférez³

2016

AiM

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Aphanizomenon ovalisporum is a cylindrospermopsin (CYN)-producing cyanobacteria species that due to its increasing worldwide distribution has become an important health alarm in the last few years. Several clusters of genes involved in CYN production have been described in different CYN + cyanobacteria genera, named aoa for Aphanizomenon and cyr for Cylindrospermopsis and others strains. The sequences of those genes are highly similar, but a rearrangement in gene order is also observed. The information on the control of CYN production by gene expression is still scarce, especially in Aphanizomenon. To obtain further information about the control of CYN production in A. ovalisporum, we have quantified the intra and extracellular CYN content, during nine days in BG11 batch cultures under optimal conditions. In parallel, the expression of four genes related to CYN synthesis, aoaA-C and cyrJ, has been analyzed by real time q-PCR. The results show a similar pattern of total CYN accumulation and gene expression. Most of the CYN is found intracellularly. Considering the high nitrogen content in the CYN molecule, we have explored if nitrogen assimilation could be related to CYN synthesis. We found inside the aoaA and aoaC sequences several putative binding domains for the global nitrogen regulator NtcA. The pattern of the ntcA expression along the culture is similar to that of CYN accumulation. Our data suggest that CYN production in A. ovalisporum seems to be controlled both by the expression of genesaoa and ntcA, this last one suggesting the influence of available nitrogen; however, other regulation mechanisms of CYN synthesis cannot be discarded.

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“…The pks (aoaC/cyrC) gene spans 5.0 kb and encodes a PKS [36]. Other studies have shown the presence of parts of aoaC/cyrC, aoaB/cyrB (and also aoaA/cyrA) genes associated with the biosynthesis of CYN in non-CYN-producing cyanobacterial strains [38,39]. Up to now, no Microcystis species has been found to produce CYN or contain any gene found in the cluster responsible for CYN biosynthesis [40].…”

Section: Discussionmentioning

confidence: 99%

Isolation and preliminary characterization of cyanobacteria strains from freshwaters of Greece

2014

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Cyanobacterial harmful algal blooms (or CyanoHABs) represent one of the most conspicuous waterborne microbial hazards. The characterization of the bloom communities remains problematic because the cyanobacterial taxonomy of certain genera has not yet been resolved. In this study, 29 planktic and benthic cyanobacterial strains were isolated from freshwaters located in Greece. The strains were assigned to the genera Chroococcus, Microcystis, Synechococcus, Jaaginema, Limnothrix, Pseudanabaena, Anabaena, and Calothrix and screened for the production of the cyanotoxins microcystins (MCs), cylindrospermopsins (CYNs), and saxitoxins (STXs) using molecular (PCR amplification of seven genes implicated in cyanotoxin biosynthesis) and immunological (ELISA) methods. This study presents, for the first time, a cyanobacteria culture collection from Greece, thus providing missing study material for the understanding of bloom formation and cyanotoxin production in the Mediterranean and for the polyphasic characterization of important components of the phytoplankton. The combined use of molecular and immunochemical methods allowed the identification of MC producing strains, but further data are needed for CYNand STX-producing cyanobacteria. The high percentage of MC-producing Microcystis strains in the urban Lakes Kastoria and Pamvotis, frequently used for agriculture irrigation, fishing and recreation, highlights the potential risk for human health.

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Occurrence of non-cylindrospermopsin-producing Aphanizomenon ovalisporum and Anabaena bergii in Lake Kinneret (Israel)

Cited by 50 publications

References 40 publications

Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Dynamics of Cylindrospermopsin Production and Toxin Gene Expression in <i>Aphanizomenon ovalisporum</i>

Isolation and preliminary characterization of cyanobacteria strains from freshwaters of Greece

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Occurrence of non-cylindrospermopsin-producing Aphanizomenon ovalisporum and Anabaena bergii in Lake Kinneret (Israel)

Cited by 50 publications

References 40 publications

Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Phylogeography of Cylindrospermopsin and Paralytic Shellfish Toxin-Producing Nostocales Cyanobacteria from Mediterranean Europe (Spain)

Dynamics of Cylindrospermopsin Production and Toxin Gene Expression in &lt;i&gt;Aphanizomenon ovalisporum&lt;/i&gt;

Isolation and preliminary characterization of cyanobacteria strains from freshwaters of Greece

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Dynamics of Cylindrospermopsin Production and Toxin Gene Expression in <i>Aphanizomenon ovalisporum</i>