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GreenWater Laboratories Potentially Toxigenic (PTOX) Cyanobacteria List

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  • Greenwater Laboratories


Some Known and Suspected Toxigenic Cyanobacteria from Around the World This list includes taxa that have had toxins identified, have been implicated in toxic events in the field, or have elicited a positive response in laboratory assays. New toxigenic cyanobacteria species are continually being discovered and data concerning known and suspected toxin producers continues to be refined and expanded. As a result, this list is by no means meant to be an exhaustive list of toxin producing cyanobacteria and their toxins.
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GreenWater Laboratories
Potentially Toxigenic (PTOX) Cyanobacteria List
Authors: Andrew Chapman & Amanda Foss
Updated: February 27, 2020
Document # 200227_PTOX
Some Known and Suspected Toxigenic Cyanobacteria from Around the World
This list includes taxa that have had toxins identified, have been implicated in toxic events in the
field, or have elicited a positive response in laboratory assays. New toxigenic cyanobacteria
species are continually being discovered and data concerning known and suspected toxin
producers continues to be refined and expanded. As a result, this list is by no means meant to be
an exhaustive list of toxin producing cyanobacteria and their toxins.
Page 2 of 13
Anagnostidinema amphibium
(previously Geitlerinema
(Borges et al., 2015) - Brazil
Anagnostidinema carotinosum
(previously Geitlerinema
Microcystins (-LY)
(Aboal, 2017) - Benthic
Anagnostidinema lemmermannii
(previously Geitlerinema
(Borges et al., 2015) - Brazil
Anabaenopsis arnoldii
(-RR, -YR, unidentified
(Mohamed and Al Shehri, 2009) Saudi Arabia
Anabaenopsis milleri
(Lanaras and Cook, 1994) Extracted from bloom, confirmed
hepatotoxic via mouse bioassay, LC-UV max abs=238-240,
likely microcystin
Anabaena spp. WA102, AL93 &
(would be classified as
Dolichospermum due to gas
vesicle presence)
(Brown et al., 2016) strain WA102; confirmed using
molecular techniques & LC-MS/MS.
(Rantala-Ylinen et al., 2011) strains 14, 37, 54, 86, 130
confirmed using molecular primers (anaC) & LC-MS/MS. All
described strains are planktonic.
Anabaena lapponica
(Spoof et al., 2006)Finland; CYN confirmed with LC-UV,
Anabaena cylindrica
(previously A. subcylindrica)
Microcystins (-YR, -LR)
(Mohamed et al., 2006)Saudi Arabia; benthic mats isolates
measured using ELISA and LC-UV after mouse bioassay
confirmed hepatotoxicity
Aphanizomenon flos-aquae &
Aph. flos-aquae/klebahnii
Anatoxin-a detected by UV/PDA (Rapala et al. (1993) but not
Cylindrospermopsin production reported by Preußel et al.,
(2009, 2006) has been contested by Oregon D. Ag. due to AFA
harvesting. Saxitoxin production was originally thought to be
Aph. flos-aquae, but the organism was reclassified to Aph. gracile
(NH) or C. issatschenkoi (China) by W. Carmichael.
Aphanizomenon gracile
STXs GTX1,4,5, STX,
(Kokociński et al., 2013)—Poland CYN confirmed in isolates
using molecular & toxin analyses (ELISA, LC-UV & MS/MS)
(Pereira et al., 2004)Portugal strain LMECYA40 isolated and
NEO & STX confirmed LC-FL (post);
US-MA lake sample dominated by Aph. gracile contained
GTX1,4, NEO & STX via LC-FL (pre)
Turkey Isolate (Yilmaz et al., 2018) had dcSTX. dcNEO, NEO,
STX, & 3 unknowns (MS/MS)
Aphanocapsa cumulus
(Domingos et al., 1999) Brazil ELISA used to screen, too low
(≤0.3 ng/mg) for LC-UV confirmation; an unidentified
spherical picoplankton was confirmed, possibly A. cumulus
Arthrospira fusiformis
(Ballot et al., 2004)Kenya isolate; MCs screened using ELISA
& confirmed with LC-UV; ANTX only LC-UV
Blennothrix lyngbyacea
Hydrocoleum lyngbyaceum)
(Méjean et al., 2010)- benthic marine associated with giant
clam poisoning event (ciguatoxins)
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Chrysosporum bergii
(previously Anabaena bergii)
(Schembri et al., 2001)Australia CYN production supported
with molecular work & LC-MS/MS
Anecdotal microcystin observation (by Adda ELISA) in bloom
dominated by C. bergii in a Texas Lake Field Collection
Chrysosporum ovalisporum
(previously Aphanizomenon
(Yilmaz et al., 2008)US-FL isolates confirmed using LC-
MS/MS, ELISA and molecular work
(Akcaalan et al., 2014)Turkey; blooms confirmed LC-MS/MS
(Banker et al., 1997) Lake Kinneret, identified using UV, MS
Cuspidothrix issatschenkoi
(previously Aphanizomenon
(Wood et al., 2007) New Zealand ANTX production
confirmed LC-MS/MS (CYN genes present, but no CYN
(Ballot et al., 2010) Germany ANTX by LC-MS/MS
(Li et al., 2003; Pereira et al., 2000) reclassification from Aph.
flos-aquae to Aph. issatschenkoi); Both studies for STXs used LC-
Cylindrospermum sp. (Finland)
(Sivonen et al., 1989)
Cylindrospermum stagnale
(Borges et al., 2015) - Brazil
Desmonostoc muscorum
(previously Nostoc muscorum)
(Mynderse et al., 1977)
(Oudra et al., 2009)Morocco
Dolichospermum circinale
(previously Anabaena circinalis)
STXs STX, GTX235, C12,
dcSTX, dcGTX3
Unknown cytotoxin
(Beltran and Neilan, 2000; Froscio et al., 2011; Pereyra et al.,
2017; Vezie et al., 1998)
Dolichospermum crassum
(previously Anabaena crassa)
(Becker et al., 2010)Brazil
Not certain if identification accurate
Dolichospermum flos-aquae
(previously Anabaena flos-
(Devlin and Edwards, 1977; Sivonen et al., 1989)
(Matsunaga et al., 1989)
(Harada et al., 1991)
Dolichospermum lemmermannii
(previously Anabaena
(Lepistö et al., 2005)
(Henriksen et al., 1997; Onodera et al., 1997)
(Onodera et al., 1997)Denmark
Oregon Bloom of D. lemmermannii produced Epi-CYN (dom)
& CYN, re-occurs annually
(Rapala et al., 2005) STX; not isolated strain
Dolichospermum macrosporum
(previously Anabaena
(Park et al., 1993) - only LC-PDA used, not confirmed
Dolichospermum mendotae
(previously Anabaena mendotae)
(Rapala et al., 1993) - only LC-PDA used, not confirmed
(Akcaalan et al., 2014)- Turkey CYN
Dolichospermum planctonicum
(previously Anabaena
(Bruno et al., 1994; Park et al., 1993)
Park et al. study only used LC-UV
Bruno et al. utilized GC-MS for derivatized ATX
Dolichospermum spiroides
(previously Anabaena spiroides)
(Park et al., 1993) (only LC-UV)
(Abreu and Ferrão-Filho, 2013) Thought to be misidentified
in other manuscripts and may be Sphaerospermopsis torques-
(Fewer et al., 2011) Finland
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Anabaena sp.
(Namikoshi et al., 1992b)
(Wang et al., 2012) - Anabaena sp. strain 90 genome, likely D.
Fischerella sp. strain CENA161
(Fiore et al., 2009)Brazil
Geitlerinema splendidum
(previously Phormidium
(-LF, -RR)
Pro-inflammatory & anti-
AChE substances
(Aboal et al., 2005)
(Rangel et al., 2014)
(Aboal, 2017) - Benthic
Gloeotrichia echinulata
(Carey et al., 2007)USA-NH; ELISA only, not confirmed
Gloeotrichia natans
(-RR & -LF)
(Aboal, 2017) - Benthic
Hapalosiphon hibernicus
(Prinsep et al., 1992)
Soil sample Hawaii (MS Thesis 2006 Philmus)
Hassallia sp.
(Vestola et al., 2014)
Heteroscytonema cf. crispum
(previously Scytonema crispum)
STXs GTX1,2,3,4,5
dcGTX23 dcSTX
(Smith et al., 2012)
Iningainema pulvinus
(McGregor and Sendall, 2017) - freshwater
Kamptonema formosum
(previously Phormidium
(Hemscheidt et al., 1995)
Leibleinia gracilis (previously
Phormidium gracile)
Hoiamide A,
(Pereira et al., 2009) marine; associated with Moorena
Leptolyngbya sp. CENA103 &
(Furtado et al., 2009) Brazil wastewater isolates, only
measured using ELISA (Beacon) at 0.14-0.31 ppb (ng/mL), no
confirmatory analysis
Leptolyngbya boryana
(previously Plectonema
(Mohamed et al., 2006) ELISA, Bioassay & HPLC (-LR, -YR)
Limnothrix redekei
(Pineda-Mendoza et al., 2012)Mexico - (low levels by ELISA
and not confirmed by other techniques
Limnothrix sp. CENA109 &
CENA110 (likely L. redekei
based on genetics)
(Furtado et al., 2009) Brazil wastewater isolates, only
measured using ELISA (Beacon) at 0.19-0.42 ppb (ng/mL), no
confirmatory analysis
Lyngbya confervoides
(Williams et al., 2002)US
Merismopedia sp. CENA106 (M.
cf. tenuissima)
(Furtado et al., 2009) Brazil wastewater isolate, only
measured using ELISA (Beacon) at 2.17 ppb (ng/mL), no
confirmatory analysis
Microcoleus autumnalis
(previously Phormidium
(Heath et al., 2010)
Microcystis aeruginosa
(Le Ai Nguyen et al., 2012)
Microcystis botrys
(Stefanelli et al., 2017)
Microcystis ichthyoblabe
(Sabour et al., 2002)
Microcystis panniformis
(Bittencourt-Oliveira et al., 2005)
Microcystis smithii
(Liu et al., 2011)- China
Microcystis viridis
(Kameyama et al., 2004; Song et al., 1998)
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Microcystis wesenbergii
(Namikoshi et al., 1992a)
Microcystis sp. (Japan)
(Park et al., 1993)-Only LC-UV used, highly suspect
Microcoleus autumnalis
(previously Phormidium
(Heath et al., 2014)
(Aboal, 2017) - Benthic
Microseira (Lyngbya) wollei
STXs - dcSTX, dcGTX23,
(Seifert et al., 2007)Australia
(Onodera et al., 1997)USA-AL
(Foss et al., 2012)USA-FL
Moorena bouillonii (previously
(Klein et al., 1999)New Guinea
Moorena producens (previously
Lyngbya majuscula)
(Capper et al., 2005; Edwards et al., 2004; Liu and Rein, 2010;
Osborne et al., 2008, 2001; Taylor et al., 2014) - marine
Nodularia sphaerocarpa
(Beattie et al., 2000) - freshwater
Nodularia spumigena
(Mazur-Marzec et al., 2013) - marine
Nostoc sp. 5/96
(Tomsickova et al., 2014)
Nostoc sp. 152
[DMAdda5] &
[ADMAdda5] MCs
(Sivonen et al., 1992)
Nostoc spp.
(Sivonen et al., 1990)
Nostoc cf. commune
(-LF, -LY)
(Teneva et al., 2012) - ?
(Aboal, 2017) - Benthic
Nostoc linckia
(Teneva et al., 2012) ?
Nostoc paludosum
(La Claire and Manning, 2015)
Nostoc carneum (previously
Nostoc spongiaeforme)
Microcystins (-YR, -LR)
(Mohamed et al., 2006)Saudi Arabia; benthic isolate
confirmed using mouse bioassay, ELISA & LC-UV
Oscillatoria limosa
(Mohamed, 2008)Saudi Arabia
Oscillatoria margaritifera
(-RR, -LF, -LY)
(Aboal, 2017) - Benthic
Oscillatoria spp.
(Cadel-Six et al., 2009)
Oscillatoria PCC 6506
Anatoxin-a (99:1)
7-epi-CYN & CYN
(Méjean et al., 2010)FR: New Caledonia, (Mazmouz et al.,
Oscillatoria tenuis
(Brittain et al., 2000)Egypt
oscillatorialean strains PCC
10601, PCC 10702, PCC 10608
(A, B, C in micrograph)
(Cadel-Six et al., 2007)
Phormidium spp.
(Izaguirre et al., 2007) Analyzed by PP1A and HPLC-PDA
and/or MS indicated MC-LR was present
Potamolinea aerugineocaerulea
(previously Phormidium
(Teneva et al., 2003) freshwater Europe
Phormidium corium
(Mohamed et al., 2006)Saudi Arabia
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Phormidium favosum
(Gugger et al., 2005)France (river)
Phormidium nigroviride
(previously Oscillatoria
(Mynderse et al., 1977) - Tropic/subtropic sea water
Phormidium willei
(Krienitz et al., 2003)
Phormidium uncinatum
(-LF, -LY)
(Borges et al., 2015)
(Aboal, 2017) - Benthic
Planktothrix agardhii
Anatoxin-a Microcystins
(Osswald et al., 2007)
(Luukkainen et al., 1993)
Planktothrix isothrix
(Bittencourt-Oliveira et al., 2014)
Planktothrix rubescens
Microcystins (Hty
(Viaggiu et al., 2004)
(Ernst et al., 2006; Niedermeyer et al., 2014)
Planktothrix sp. FP1
(Pomati et al., 2000)Italy- identification based on genetics
which may support novo status; pre- & post-column oxidation
Pseudanabaena galeata
(Oudra et al., 2002) benthic LC-UV/PDA & ELISA
Pseudanabaena mucicola
(Oudra et al., 2002) planktonic - LC-UV/PDA &ELISA
Pseudanabaena limnetica
(Marsalek et al., 2003)Czech Repub. not unialgal LC-
Pseudocapsa dubia
(-RR, -YR)
(Cantoral Uriza et al., 2017) - Benthic
Radiocystis fernandoi
(Vieira et al., 2003)
Raphidiopsis curvata
(Eaglesham et al., 2003)
Raphidiopsis brookii
(Yunes et al., 2009) Sub tropical
Raphidiopsis mediterranea
(Hodoki et al., 2013)
(Watanabe et al., 2003)
(McGregor et al., 2011)
Raphidiopsis raciborskii
(previously Cylindrospermopsis
2,3,56, dcNEO
(Vehovszky et al., 2009) Hungary; only single quad MS used
after + neuronal effect (snail neurons) for ATX/HTX
(Schembri et al., 2001)Australia confirmed CYN in isolates
molecular & LC-MS/MS
(Lagos et al., 1999; Miotto et al., 2017)Brazil mouse
bioassay, LC-FL & MS on isolates
Rivularia biasolettiana
(-RR, -LR, -LY)
(Aboal et al., 2005)
(Cantoral Uriza et al., 2017)
Rivularia haematites
(Aboal et al., 2005)
Romeria caruaru
(Komárek et al., 2001)
Schizothrix calcicola
(Mynderse et al., 1977)
Scytonematopsis crustacea
(previously Calothrix crustacea)
(Mynderse et al., 1977)
Scytonema drilosiphon
(Cantoral Uriza et al., 2017) - Benthic
Page 7 of 13
Scytonema ocellatum
(antineoplastic &
(Ishibashi et al., 1986)
Scytonema pseudohofmannii
(antineoplastic &
(Ishibashi et al., 1986)
Snowella lacustris
(Sant’Anna and Azevedo, 2000)—Brazil
aphanizomenoides (previously
Anabaena and Aphanizomenon)
(Bittencourt-Oliveira et al., 2011) potential CYN & STX
producer Brazil
(Sabour et al., 2005) MC production questioned by (Cirés
and Ballot, 2016)
Sphaerospermopsis torques-
reginae (previously Anabaena)
(Dörr et al., 2010) Originally published as T? Anabaena
spiroides, Anabaena oumiana, changed to Sphaerospermopsis
oumiana and is now Sphaerospermopsis torques-reginae
Stenomitos frigidus (previously
Pseudanabaena frigida)
(Aboal, 2017) - Benthic
Symploca muscorum
(Mynderse et al., 1977)
Synechococcus sp.
(Carmichael and Li, 2006) - marine
Synechococcus sp. CENA108
(Furtado et al., 2009) Brazil wastewater isolate, only
measured using ELISA (Beacon) at 0.22 ppb (ng/mL), no
confirmatory analysis
Synechocystis sp.
(Oudra et al., 2002) UV PDA only
Synechocystis sp. PCC 6803
(Bi et al., 2011)
Synechocystis aquatilis
(Domingos et al., 1999) Brazil, brackish lagoon isolate
Tolypothrix conglutinata
(antineoplastic &
(Ishibashi et al., 1986)
Tolypothrix distorta
(Aboal et al., 2005)
Trichodesmium erythraeum
Aplysiatoxins (5 variants)
(Gupta et al., 2014; Ramos et al., 2005) brackish, marine
Trichodesmium thiebautii
Trichotoxin 2 - neurotoxin
(Schock et al., 2011) brackish, marine
Trichormus variabilis
(previously Anabaena)
Microcystin (-YR, -LR)
(Mohamed et al., 2006)Saudi Arabia, benthic mat isolate
toxic via mouse bioassay, MCs by ELISA and LC-UV
Tychonema bourrellyi
(Shams et al., 2015)
Umezakia natans
(Harada et al., 1994)
Woronichinia naegeliana
(Bober et al., 2011) trace MC-LR
Page 8 of 13
Aboal, M., Puig, M.Á., Asencio, A.D., 2005. Production of microcystins in calcareous Mediterranean streams: The Alharabe River,
Segura River basin in south-east Spain. J. Appl. Phycol. 17, 231243.
Abreu, F.Q. de, Ferrão-Filho, A. da S., 2013. Effects of an Anatoxin-a(s)-Producing Strain of Anabaena spiroides (Cyanobacteria) on the
Survivorship and Somatic Growth of Two Daphnia similis Clones. J. Environ. Prot. (Irvine,. Calif). 04, 1218.
Akcaalan, R., Köker, L., Oğuz, A., Spoof, L., Meriluoto, J., Albay, M., 2014. First report of cylindrospermopsin production by two
cyanobacteria (Dolichospermum mendotae and Chrysosporum ovalisporum ) in Lake Iznik, Turkey. Toxins (Basel). 6, 31733186.
Ballot, A., Fastner, J., Lentz, M., Wiedner, C., 2010. First report of anatoxin-a-producing cyanobacterium Aphanizomenon issatschenkoi in
northeastern Germany. Toxicon 56, 964971.
Ballot, A., Krienitz, L., Kotut, K., Wiegand, C., Metcalf, J.S., Codd, G. a., Pflugmacher, S., 2004. Cyanobacteria and cyanobacterial toxins
in three alkaline Rift Valley lakes of Kenya - Lakes Bogoria, Nakuru and Elmenteita. J. Plankton Res. 26, 925935.
Banker, R., Carmeli, S., Hadas, O., Teltsch, B., Porat, R., Sukenik, A., 1997. Identification of Cylindrospermopsin in Aphanizomenon
Ovalisporum (Cyanophyceae) Isolated From Lake Kinneret, Israel1. J. Phycol. 33, 613616.
Beattie, K.A., Kaya, K., Codd, G.A., 2000. The cyanobacterium Nodularia PCC 7804, of freshwater origin, produces [L-Har2]nodularin.
Phytochemistry 54, 5761.
Becker, V., Ihara, P., Yunes, J.S., Huszar, V.L.M., 2010. Occurrence of anatoxin-a(s) during a bloom of Anabaena crassa in a water-supply
reservoir in southern Brazil. J. Appl. Phycol. 22, 235241.
Beltran, E.C., Neilan, B. a., 2000. Geographical segregation of the neurotoxin-producing cyanobacterium Anabaena circinalis. Appl.
Environ. Microbiol. 66, 44684474.
Bi, S., Wang, W., Zhao, Y., Ru, S., Liu, Y., 2011. Studies on hemolysis of hemolysin produced by Synechocystis sp. PCC 6803. J. Ocean
Univ. China 10, 362368.
Bittencourt-Oliveira, M. do C., Piccin-Santos, V., Kujbida, P., Moura, A. do N., 2011. Cylindrospermopsin in Water Supply Reservoirs in
Brazil Determined by Immunochemical and Molecular Methods. J. Water Resour. Prot. 03, 349355.
Bittencourt-Oliveira, M.D.C., Kujbida, P., Cardozo, K.H.M., Carvalho, V.M., Moura, A.D.N., Colepicolo, P., Pinto, E., 2005. A novel
rhythm of microcystin biosynthesis is described in the cyanobacterium Microcystis panniformis Komarek et al. Biochem. Biophys.
Res. Commun. 326, 687694.
Bittencourt-Oliveira, M.D.C., Piccin-Santos, V., Moura, A.N., Aragão-Tavares, N.K.C., Cordeiro-Araújo, M.K., 2014. Cyanobacteria,
microcystins and cylindrospermopsin in public drinking supply reservoirs of Brazil. An. Acad. Bras. Cienc. 86, 297309.
Bober, B., Lechowski, Z., Bialczyk, J., 2011. Determination of some cyanopeptides synthesized by Woronichinia naegeliana
(Chroococcales, Cyanophyceae). Phycol. Res. 59, 286294.
Borges, H.L.F., Branco, L.H.Z., Martins, M.D., Lima, C.S., Barbosa, P.T., Lira, G.A.S.T., Bittencourt-Oliveira, M.C., Molica, R.J.R., 2015.
Cyanotoxin production and phylogeny of benthic cyanobacterial strains isolated from the northeast of Brazil. Harmful Algae 43,
Brittain, S., Mohamed, Z.A., Wang, J., Lehmann, V.K.B., Carmichael, W.W., Rinehart, K.L., 2000. Isolation and characterization of
microcystins from a River Nile strain of Oscillatoria tenuis Agardh ex Gomont. Toxicon 38, 17591771.
Brown, N.M., Mueller, R.S., Shepardson, J.W., Landry, Z.C., Morré, J.T., Maier, C.S., Hardy, F.J., Dreher, T.W., 2016. Structural and
functional analysis of the finished genome of the recently isolated toxic Anabaena sp. WA102. BMC Genomics 17, 457.
Bruno, M., Barbini, D.A., Pierdominici, E., Serse, A.P., Ioppolo, A., 1994. Anatoxin-a and a previously unknown toxin in Anabaena
planctonica from blooms found in Lake Mulargia (Italy). Toxicon 32, 369373.
Cadel-Six, S., Iteman, I., Peyraud-Thomas, C., Mann, S., Ploux, O., Méjean, A., 2009. Identification of a polyketide synthase coding
sequence specific for anatoxin-a-producing Oscillatoria cyanobacteria. Appl. Environ. Microbiol. 75, 49094912.
Cadel-Six, S., Peyraud-Thomas, C., Brient, L., De Marsac, N.T., Rippka, R., Méjean, A., 2007. Different genotypes of anatoxin-producing
cyanobacteria coexist in the Tarn River, France. Appl. Environ. Microbiol. 73, 76057614.
Cantoral Uriza, E.A., Asencio, A.D., Aboal, M., 2017. Are we underestimating benthic cyanotoxins? extensive sampling results from
Spain. Toxins (Basel). 9.
Page 9 of 13
Capper, A., Tibbetts, I.R., O'Neil, J.M., Shaw, G.R., 2005. The fate of Lyngbya majuscula toxins in three potential consumers. J.
Chem. Ecol. 31, 15951606.
Carey, C.C., Haney, J.F., Cottingham, K.L., 2007. First report of microcystin-LR in the cyanobacterium Gloeotrichia echinulata. Environ.
Toxicol. 22, 337339.
Carmichael, W.W., Li, R., 2006. Cyanobacteria toxins in the Salton Sea. Saline Systems 2, 5.
Cirés, S., Ballot, A., 2016. A review of the phylogeny, ecology and toxin production of bloom-forming Aphanizomenon spp. and related
species within the Nostocales (cyanobacteria). Harmful Algae.
Devlin, J., Edwards, O., 1977. Anatoxin-a, a toxic alkaloid from Anabaena flos-aquae NRC-44h. Can. J. Chem. 15.
Domingos, P., Rubim, T.K., Molica, R.J.R., Azevedo, S.M.F.O., Carmichael, W.W., 1999. First report of microcystin production by
picoplanktonic cyanobacteria isolated from a northeast Brazilian drinking water supply. Environ. Toxicol. 14, 3135.
Dörr, F.A., Rodríguez, V., Molica, R., Henriksen, P., Krock, B., Pinto, E., 2010. Methods for detection of anatoxin-a(s) by liquid
chromatography coupled to electrospray ionization-tandem mass spectrometry. Toxicon 55, 9299.
Eaglesham, G.K., Li, R., Watanabe, M.M., Brittain, S., Liu, Y., Carmichael, W.W., Shaw, G.R., 2003. First report of the cyanotoxins
cylindrospermopsin and dexycylindrospermopsin from Raphidiopsis curvata (Cyanobacteria). J. Phycol. 37, 11211126.
Edwards, D.J., Marquez, B.L., Nogle, L.M., McPhail, K., Goeger, D.E., Roberts, M.A., Gerwick, W.H., 2004. Structure and Biosynthesis of
the Jamaicamides, New Mixed Polyketide-Peptide Neurotoxins from the Marine Cyanobacterium Lyngbya majuscula. Chem. Biol.
11, 817833.
Ernst, B., Hoeger, S.J., O’Brien, E., Dietrich, D.R., 2006. Oral toxicity of the microcystin-containing cyanobacterium Planktothrix rubescens
in European whitefish (Coregonus lavaretus). Aquat. Toxicol. 79, 3140.
Fewer, D.P., Halinen, K., Sipari, H., Bernardová, K., Mänttäri, M., Eronen, E., Sivonen, K., 2011. Non-autonomous transposable
elements associated with inactivation of microcystin gene clusters in strains of the genus Anabaena isolated from the Baltic Sea.
Environ. Microbiol. Rep. 3, 189194.
Fiore, M.F., Genuário, D.B., da Silva, C.S.P., Shishido, T.K., Moraes, L.A.B., Neto, R.C., Silva-Stenico, M.E., 2009. Microcystin production
by a freshwater spring cyanobacterium of the genus Fischerella. Toxicon 53, 754761.
Foss, A., Phlips, E., Aubel, M., Szabo, N., 2012. Investigation of extraction and analysis techniques for Lyngbya wollei derived Paralytic
Shellfish Toxins. Toxicon 60, 11481158.
Froscio, S., Sieburn, K., Lau, H.M., Humpage, A., 2011. Novel cytotoxicity associated with Anabaena circinalis 131C. Toxicon 58, 689692.
Furtado, A.L.F.F., Calijuri, M.D.C., Lorenzi, A.S., Honda, R.Y., Genuário, D.B., Fiore, M.F., 2009. Morphological and molecular
characterization of cyanobacteria from a Brazilian facultative wastewater stabilization pond and evaluation of microcystin
production. Hydrobiologia 627, 195209.
Gugger, M., Lenoir, S., Berger, C., Ledreux, A., Druart, J.-C., Humbert, J.-F., Guette, C., Bernard, C., 2005. First report in a river in
France of the benthic cyanobacterium Phormidium favosum producing anatoxin-a associated with dog neurotoxicosis. Toxicon 45,
Gupta, D., Kaur, P., Leong, S., Tan, L., Prinsep, M., Chu, J., 2014. Anti-Chikungunya Viral Activities of Aplysiatoxin-Related
Compounds from the Marine Cyanobacterium Trichodesmium erythraeum. Mar. Drugs 12, 115127.
Harada, K., Ohtani, I., Iwamoto, K., Suzuki, M., Watanabe, M.F., Watanabe, M., Terao, K., 1994. Isolation of cylindrospermopsin from a
cyanobacterium Umezakia natans and its screening method. Toxicon 32, 7384.
Harada, K.I., Ogawa, K., Kimura, Y., Murata, H., Suzuki, M., Thorn, P.M., Evans, W.R., Carmichael, W.W., 1991. Microcystins from
Anabaena flos-aquae NRC 525-17. Chem. Res. Toxicol. 4, 535540.
Heath, M.W., Wood, S.A., Barbieri, R.F., Young, R.G., Ryan, K.G., 2014. Effects of nitrogen and phosphorus on anatoxin-a,
homoanatoxin-a, dihydroanatoxin-a and dihydrohomoanatoxin-a production by Phormidium autumnale. Toxicon.
Heath, M.W., Wood, S.A., Ryan, K.G., 2010. Polyphasic assessment of fresh-water benthic mat-forming cyanobacteria isolated from
New Zealand. FEMS Microbiol. Ecol. 73, 95109.
Hemscheidt, T., Rapala, J., Sivonen, K., Skulberg, O.M., 1995. Biosynthesis os anatoxin-a in Anabaena flos-aquae and homoanatoxin-a in
Oscillatoria formosa. J. Chem. Soc. 13, 13611362.
Henriksen, P., Carmichael, W.W., Jisi, A., Moestrup, Ø., 1997. Detection of an anatoxin-a(s)-like anticholinesterase in natural blooms
Page 10 of 13
and cultures of cyanobacteria/blue-green algae from Danish lakes and in the stomach content of poisoned birds. Toxicon 35, 901
Hodoki, Y., Ohbayashi, K., Kobayashi, Y., Takasu, H., Okuda, N., Nakano, S., 2013. Anatoxin-a-producing Raphidiopsis mediterranea
Skuja var. grandis Hill is one ecotype of non-heterocytous Cuspidothrix issatschenkoi (Usačev) Rajaniemi et al. in Japanese lakes.
Harmful Algae 21, 4453.
Ishibashi, M., Moore, R.E., Patterson, G.M.L., Xu, C., Clardy, J., 1986. Scytophycins, cytotoxic and antimycotic agents from the
cyanophyte Scytonema pseudohofmanni. J. Org. Chem. 51, 53005306.
Izaguirre, G., Jungblut, A.-D.D., Neilan, B.A., 2007. Benthic cyanobacteria (Oscillatoriaceae) that produce microcystin-LR, isolated from
four reservoirs in southern California. Water Res. 41, 492498.
Kameyama, K., Sugiura, N., Inamori, Y., Maekawa, T., 2004. Characteristics of microcystin production in the cell cycle of Microcystis
viridis. Environ. Toxicol. 19, 2025.
Klein, D., Braekman, J.-C., Daloze, D., Hoffmann, L., Castillo, G., Demoulin, V., 1999. Lyngbyapeptin A, a modified tetrapeptide from
Lyngbya bouillonii (Cyanophyceae). Tetrahedron Lett. 40, 695696.
Kokociński, M., Mankiewicz-Boczek, J., Jurczak, T., Spoof, L., Meriluoto, J., Rejmonczyk, E., Hautala, H., Vehniäinen, M., Pawełczyk, J.,
Soininen, J., 2013. Aphanizomenon gracile (Nostocales), a cylindrospermopsin-producing cyanobacterium in Polish lakes. Environ.
Sci. Pollut. Res. 20, 52435264.
Komárek, J., Azevedo, M.T.D.P., Domingos, P., Komárková, J., Tichý, M., 2001. Background of the Caruaru tragedy: a case taxonomic
study of toxic cyanobacteria. Arch. Hydrobiol. Suppl. Algol. Stud. 103, 929.
Krienitz, L., Ballot, A., Kotut, K., Wiegand, C., Pütz, S., Metcalf, J.S., Codd, G.A., Pflugmacher, S., 2003. Contribution of hot spring
cyanobacteria to the mysterious deaths of Lesser Flamingos at Lake Bogoria, Kenya. FEMS Microbiol. Ecol. 43, 141148.
La Claire, J.W., Manning, S.R., 2015. Ichthyotoxins, Phycotoxins.
Lagos, N., Onodera, H., Zagatto, P.A., Andrinolo, D., Azevedo, S.M.F.Q., Oshima, Y., 1999. The first evidence of paralytic shellfish
toxins in the freshwater cyanobacterium Cylindrospermopsis raciborskii, isolated from Brazil. Toxicon 37, 13591373.
Lanaras, T., Cook, C.M., 1994. Toxin extraction from an Anabaenopsis milleri - Dominated bloom. Sci. Total Environ. 142, 163169.
Le Ai Nguyen, V., Tanabe, Y., Matsuura, H., Kaya, K., Watanabe, M.M., 2012. Morphological, biochemical and phylogenetic
assessments of water-bloom-forming tropical morphospecies of Microcystis (Chroococcales, Cyanobacteria). Phycol. Res. 60, 208
Lepistö, L., Rapala, J., Lyra, C., Berg, K.A., Erkomaa, K., Issakainen, J., 2005. Occurrence and toxicity of cyanobacterial blooms
dominated by Anabaena lemmermannii P. Richter and Aphanizomenon spp. in boreal lakes in 2003. Arch. Hydrobiol. Suppl. Algol.
Stud. 117, 315328.
Li, R., Carmichael, W.W., Pereira, P., 2003. Morphological and 16s rRNA gene evidence for reclassification of the paralytic shellfish
toxin producing Aphanizomenon flos-aquae LMECYA 31 as Aphanizomenon issatschenkoi (Cyanophyceae). J. Phycol. 39, 814818.
Liu, L., Rein, K.S., 2010. New peptides isolated from Lyngbya species: A review. Mar. Drugs.
Liu, Y., Tan, W., Wu, X., Wu, Z., Yu, G., Li, R., 2011. First report of microcystin production in Microcystis smithii Komorek and
Anagnostidis (Cyanobacteria) from a water bloom in Eastern China. J. Environ. Sci. 23, 102107.
Luukkainen, R., Sivonen, K., Namikoshi, M., Fardig, M., Rinehart, K.L., Niemela, S.I., 1993. Isolation and identification of eight
microcystins from thirteen Oscillatoria agardhii strains and structure of a new microcystin. Appl. Environ. Microbiol. 59, 2204
Marsalek, B., Blaha, L., Babica, P., 2003. Analyses of microcystins in the biomass of Pseudanabaena limnetica collected in Znojmo
reservoir. Czech Phycol. 3, 195197.
Matsunaga, S., Moore, R.E., Niemczura, W.P., Carmichael, W.W., 1989. Anatoxin-a(s), a potent anticholinesterase from Anabaena flos-
aquae. J. Am. Chem. Soc. 111, 80218023.
Mazmouz, R., Chapuis-Hugon, F., Mann, S., Pichon, V., Méjean, A., Ploux, O., 2010. Biosynthesis of cylindrospermopsin and 7-
epicylindrospermopsin in Oscillatoria sp. strain PCC 6506: Identification of the cyr gene cluster and toxin analysis. Appl. Environ.
Microbiol. 76, 49434949.
Mazur-Marzec, H., Kaczkowska, M.J., Blaszczyk, A., Akcaalan, R., Spoof, L., Meriluoto, J., 2013. Diversity of peptides produced by
Page 11 of 13
Nodularia spumigena from various geographical regions. Mar. Drugs 11, 119.
McGregor, G., Sendall, B., Hunt, L., Eaglesham, G., 2011. Report of the cyanotoxins cylindrospermopsin and deoxy-cylindrospermopsin
from Raphidiopsis mediterranea Skuja (Cyanobacteria/Nostocales). Harmful Algae.
McGregor, G.B., Sendall, B.C., 2017. Iningainema pulvinus gen nov., sp nov. (Cyanobacteria, Scytonemataceae) a new nodularin producer
from Edgbaston Reserve, north-eastern Australia. Harmful Algae 62, 1019.
Méjean, A., Peyraud-Thomas, C., Kerbrat, A.S., Golubic, S., Pauillac, S., Chinain, M., Laurent, D., 2010. First identification of the
neurotoxin homoanatoxin-a from mats of Hydrocoleum lyngbyaceum (marine cyanobacterium) possibly linked to giant clam
poisoning in New Caledonia. Toxicon 56, 829835.
Miotto, M.C., Costa, L.D.F., Brentano, D.M., Nader, C., Dos Santos Souza, L., Gressler, P.D., Laudares-Silva, R., Yunes, J.S., Barufi, J.B.,
Rörig, L.R., 2017. Ecophysiological characterization and toxin profile of two strains of Cylindrospermopsis raciborskii isolated from a
subtropical lagoon in Southern Brazil. Hydrobiologia 117.
Mohamed, Z. a., Al Shehri, A.M., 2009. Microcystin-producing blooms of Anabaenopsis arnoldi in a potable mountain lake in Saudi
Arabia: Research article. FEMS Microbiol. Ecol. 69, 98105.
Mohamed, Z.A., 2008. Toxic cyanobacteria and cyanotoxins in public hot springs in Saudi Arabia. Toxicon 51, 1727.
Mohamed, Z.A., El-Sharouny, H.M., Ali, W.S.M., 2006. Microcystin production in benthic mats of cyanobacteria in the Nile River and
irrigation canals, Egypt. Toxicon 47, 584590.
Mynderse, J., Moore, R., Kashiwagi, M., Norton, T., 1977. Antileukemia activity in the Osillatoriaceae: isolation of Debromoaplysiatoxin
from Lyngbya. Science (80-. ). 196.
Namikoshi, M., Kenneth, L., Sakai, R., Stotts, R.R., Dahlem, A.M., Beasley, V.R., Carmichael, W.W., Evans, W.R., 1992a. Identification of
12 hepatotoxins from a Homer Lake bloom of the cyanobacteria Microcystis aeruginosa, Microcystis viridis, and Microcystis
wesenbergii: nine new microcystins. J. Or 57, 866872.
Namikoshi, M., Sivonen, K., Evans, W.R., Carmichael, W.W., Sun, F., Rouhiainen, L., Luukkainen, R., Rinehart, K.L., 1992b. Two new L-
serine variants of microcystins-LR and -RR from Anabaena sp. strains 202 A1 and 202 A2. Toxicon 30, 14571464.
Niedermeyer, T.H.J., Schmieder, P., Kurmayer, R., 2014. Isolation of microcystins from the cyanobacterium Planktothrix rubescens strain
No80. Nat. Products Bioprospect. 4, 3745.
Onodera, H., Oshima, Y., Henriksen, P., Yasumoto, T., 1997. Confirmation of anatoxin-a(s), in the cyanobacterium Anabaena
lemmermannii, as the cause of bird kills in Danish lakes. Toxicon 35, 16451648.
Osborne, N., Seawright, A., Shaw, G., 2008. Dermal toxicology of Lyngbya majuscula, from Moreton Bay, Queensland, Australia.
Harmful Algae 7, 584589.
Osborne, N.J.T., Webb, P.M., Shaw, G.R., 2001. The toxins of Lyngbya majuscula and their human and ecological health effects. Environ.
Int. 27, 381392.
Osswald, J., Rellán, S., Gago, A., Vasconcelos, V., 2007. Toxicology and detection methods of the alkaloid neurotoxin produced by
cyanobacteria, anatoxin-a. Environ. Int. 33, 10701089.
Oudra, B., Dadi-El Andaloussi, M., Vasconcelos, V.M., 2009. Identification and quantification of microcystins from a Nostoc muscorum
bloom occurring in Oukaïmeden River (High-Atlas mountains of Marrakech, Morocco). Environ. Monit. Assess. 149, 437444.
Oudra, B., Loudiki, M., Vasconcelos, V., Sabour, B., Sbiyyaa, B., Oufdou, K., Mezrioui, N., 2002. Detection and quantification of
microcystins from cyanobacteria strains isolated from reservoirs and ponds in Morocco. Environ. Toxicol. 17, 3239.
Park, H.-D., Watanabe, M.F., Harada, K.-I., Nagai, H., Suzuki, M., Watanabe, M., Hayashi, H., 1993. Hepatotoxin (microcystin) and
neurotoxin (anatoxin-a) contained in natural blooms and strains of cyanobacteria from Japanese freshwaters. Nat. Toxins 1, 353
Pereira, A., Cao, Z., Murray, T.F., Gerwick, W.H., 2009. Hoiamide A, a Sodium Channel Activator of Unusual Architecture from a
Consortium of Two Papua New Guinea Cyanobacteria. Chem. Biol. 16, 893906.
Pereira, P., Li, R., Carmichael, W.W., Dias, E., Franca, S., 2004. Taxonomy and production of paralytic shellfish toxins by the freshwater
cyanobacterium Aphanizomenon gracile LMECYA40. Eur. J. Phycol. 39, 361368.
Pereira, P., Onodera, H., Andrinolo, D., Franca, S., Ara??jo, F., Lagos, N., Oshima, Y., 2000. Paralytic shellfish toxins in the freshwater
cyanobacterium Aphanizomenon flos-aquae, isolated from Montargil reservoir, Portugal. Toxicon 38, 16891702.
Page 12 of 13
Pereyra, J.P.A., D’Agostino, P.M., Mazmouz, R., Woodhouse, J.N., Pickford, R., Jameson, I., Neilan, B.A., 2017. Molecular and
morphological survey of saxitoxin-producing cyanobacterium Dolichospermum circinale (Anabaena circinalis) isolated from
geographically distinct regions of Australia. Toxicon 138, 6877.
Pineda-Mendoza, R.M., Olvera-Ramírez, R., Martínez-Jerónimo, F., 2012. Microcystins produced by filamentous cyanobacteria in urban
lakes. A case study in Mexico City. Hidrobiologica 22, 290298.
Pomati, F., Sacchi, S., Rossetti, C., Giovannardi, S., Onodera, H., Oshima, Y., Neilan, B.A., 2000. The freshwater cyanobacterium
Planktothrix sp. FP1: Molecular identification and detection of paralytic shellfish toxins. J. Phycol. 36, 553562.
Preußel, K., Stüken, A., Wiedner, C., Chorus, I., Fastner, J., 2006. First report on cylindrospermopsin producing Aphanizomenon flos-
aquae (Cyanobacteria) isolated from two German lakes. Toxicon 47, 156162.
Preußel, K., Wessel, G., Fastner, J., Chorus, I., 2009. Response of cylindrospermopsin production and release in Aphanizomenon flos-aquae
(Cyanobacteria) to varying light and temperature conditions. Harmful Algae 8, 645650.
Prinsep, M.R., Caplan, F.R., Moore, R.E., Patterson, G.M.L., E. Honkanen, R., Boynton, A.L., 1992. Microcystin-LA from a blue-green
alga belonging to the Stigonematales. Phytochemistry 31, 12471248.
Ramos, A.G., Martel, A., Codd, G.A., Soler, E., Coca, J., Redondo, A., Morrison, L.F., Metcalf, J.S., Ojeda, A., Suárez, S., Petit, M., 2005.
Bloom of the marine diazotrophic cyanobacterium Trichodesmium erythraeum in the Northwest African Upwelling. Mar. Ecol.
Prog. Ser. 301, 303305.
Rangel, M., Martins, J.C.G., Garcia, A.N., Conserva, G.A.A., Costa-Neves, A., Sant’Anna, C.L., De Carvalho, L.R., 2014. Analysis of the
toxicity and histopathology induced by the oral administration of Pseudanabaena galeata and Geitlerinema splendidum
(Cyanobacteria) extracts to mice. Mar. Drugs 12, 508524.
Rantala-Ylinen, A., Känä, S., Wang, H., Rouhiainen, L., Wahlsten, M., Rizzi, E., Berg, K., Gugger, M., Sivonen, K., 2011. Anatoxin-a
synthetase gene cluster of the cyanobacterium Anabaena sp. strain 37 and molecular methods to detect potential producers. Appl.
Environ. Microbiol. 77, 72717278.
Rapala, J., Robertson, A., Negri, A.P., Berg, K.A., Tuomi, P., Lyra, C., Erkomaa, K., Lahti, K., Hoppu, K., Lepistö, L., 2005. First report of
saxitoxin in Finnish lakes and possible associated effects on human health, in: Environmental Toxicology. pp. 331340.
Rapala, J., Sivonen, K., Luukkainen, R., Niemela, S.I., 1993. Anatoxin-a concentration in Anabaena and Aphanizomenon under different
environmental conditions and comparison of growth by toxic and non-toxic Anabaena-strains - a laboratory study. Appl. Phycol.
5, 581591.
Sabour, B., Loudiki, M., Oudra, B., Oubraim, S., Fawzi, B., Fadlaoui, S., Chlaida, M., Vasconcelos, V., 2002. First results on Microcystis
ichthyoblabe Kutz. toxic bloom in the hypertrophic Oued Mellah reservoir (Morocco). Ann. Limnol. J. Limnol.
Sabour, B., Loudiki, M., Oudra, B., Vasconcelos, V., Oubraim, S., Fawzi, B., 2005. Dynamics and toxicity of Anabaena aphanizomenoides
(Cyanobacteria) waterblooms in the shallow brackish Oued Mellah lake (Morocco). Aquat. Ecosyst. Heal. Manag. 8, 95104.
Sant’Anna, C.L., Azevedo, M.T. De, 2000. Contribution to the knowledge of potentially toxic Cyanobacteria from Brazil. Nov. Hedwigia
71, 359385.
Schembri, M. a, Neilan, B. a, Saint, C.P., Christopher, P., Saint, C.P., 2001. Identification of genes implicated in toxin production in the
cyanobacterium Cylindrospermopsis raciborskii. Environ. Toxicol. 16, 413421.
Schock, T.B., Huncik, K., Beauchesne, K.R., Villareal, T.A., Moeller, P.D.R., 2011. Identification of Trichotoxin, a Novel Chlorinated
Compound Associated with the Bloom Forming Cyanobacterium, Trichodesmium thiebautii. Environ. Sci. Technol. 45, 75037509.
Seifert, M., McGregor, G., Eaglesham, G., Wickramasinghe, W., Shaw, G., 2007. First evidence for the production of cylindrospermopsin
and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium, Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck.
Harmful Algae 6, 7380.
Shams, S., Capelli, C., Cerasino, L., Ballot, A., Dietrich, D.R., Sivonen, K., Salmaso, N., 2015. Anatoxin-a producing Tychonema
(cyanobacteria) in European waterbodies. Water Res. 69, 6879.
Sivonen, K., Carmichael, W.W., Namikoshi, M., Rinehart, K.L., Dahlem, A.M., Niemelä, S.I., 1990. Isolation and characterization of
hepatotoxic microcystin homologs from the filamentous freshwater cyanobacterium Nostoc sp. strain 152. Appl. Environ.
Microbiol. 56, 26502657.
Sivonen, K., Himberg, K., Luukkainen, R., Niemelä, S.I., Poon, G.K., Codd, G.A., 1989. Preliminary characterization of neurotoxic
cyanobacteria blooms and strains from Finland. Toxic. Assess. 4, 339352.
Page 13 of 13
Sivonen, K., Namikoshi, M., Evans, W.R., Färdig, M., Carmichael, W.W., Rinehart, K.L., 1992. Three new microcystins, cyclic
heptapeptide hepatotoxins, from Nostoc sp. strain 152. Chem. Res. Toxicol. 5, 464469.
Smith, F.M.J., Wood, S.A., Wilks, T., Kelly, D., Broady, P.A., Williamson, W., Gaw, S., 2012. Survey of Scytonema (cyanobacteria) and
associated saxitoxins in the littoral zone of recreational lakes in Canterbury, New Zealand. Phycologia 51, 542551.
Song, L., Sano, T., Li, R., Watanabe, M.M., Liu, Y., Kaya, K., 1998. Microcystin production of Microcystis viridis (cyanobacteria) under
different culture conditions. Phycol. Res. 46, 1923.
Spoof, L., Berg, K.A., Rapala, J., Lahti, K., Lepistö, L., Metcalf, J.S., Codd, G.A., Meriluoto, J., 2006. First observation of
cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environ. Toxicol. 21, 552560.
Stefanelli, M., Scardala, S., Cabras, P.A., Orrù, A., Vichi, S., Testai, E., Funari, E., Manganelli, M., 2017. Cyanobacterial dynamics and
toxins concentrations in Lake Alto Flumendosa, Sardinia, Italy. Adv. Oceanogr. Limnol. 8.
Taylor, M.S., Stahl-Timmins, W., Redshaw, C.H., Osborne, N.J., 2014. Toxic alkaloids in Lyngbya majuscula and related tropical marine
cyanobacteria. Harmful Algae 31, 18.
Teneva, I., Asparuhova, D., Dzhambazov, B., Mladenov, R., Schirmer, K., 2003. The freshwater cyanobacterium Lyngbya aerugineo-
coerulea produces compounds toxic to mice and to mammalian and fish cells. Environ. Toxicol. 18, 920.
Teneva, I., Stoyanov, P., Belkinova, D., 2012. Production of cyanobacterial toxins from two Nostoc species (Nostocales) and evaluation of
their cytotoxicity in vitro. J. BioSci. Biotec 1, 3343.
Tomsickova, J., Ondrej, M., Cerny, J., Hrouzek, P., Kopecky, J., 2014. Analysis and Detection of Scytophycin Variants by HPLC-ESI-MS.
Chem. Nat. Compd. 49, 11701171.
Vehovszky, Á., Ács, A., Kovacs, A.W., Szabó, H., Gyori, J., Farkas, A., 2009. Isolated strains of Cylindrospermopsis raciborskii from Lake
Balaton (Hungary) produce anatoxin-a like neurotoxins. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 153, S88.
Vestola, J., Shishido, T.K., Jokela, J., Fewer, D.P., Aitio, O., Permi, P., Wahlsten, M., Wang, H., Rouhiainen, L., Sivonen, K., 2014.
Hassallidins, antifungal glycolipopeptides, are widespread among cyanobacteria and are the end-product of a nonribosomal
pathway. Proc. Natl. Acad. Sci. 111, E1909E1917.
Vezie, C., Brient, L., Sivonen, K., Bertru, G., Lefeuvre, J.C., Salkinoja-Salonen, M., 1998. Variation of microcystin content of
cyanobacterial blooms and isolated strains in Lake Grand-Lieu (France). Microb. Ecol. 35, 126135.
Viaggiu, E., Melchiorre, S., Volpi, F., Di Corcia, A., Mancini, R., Garibaldi, L., Crichigno, G., Bruno, M., 2004. Anatoxin-a toxin in the
cyanobacterium Planktothrix rubescens from a fishing pond in northern Italy. Environ. Toxicol. 19, 191197.
Vieira, J.M. dos S., Azevedo, M.T.D.P., De Oliveira Azevedo, S.M.F., Honda, R.Y., Corrêa, B., 2003. Microcystin production by
Radiocystis fernandoi (Chroococcales, Cyanobacteria) isolated from a drinking water reservoir in the city of Belém, PA, Brazilian
Amazonia region. Toxicon 42, 709713.
Wang, H., Sivonen, K., Rouhiainen, L., Fewer, D.P., Lyra, C., Rantala-Ylinen, A., Vestola, J., Jokela, J., Rantasärkkä, K., Li, Z., Liu, B.,
2012. Genome-derived insights into the biology of the hepatotoxic bloom-forming cyanobacterium Anabaena sp. strain 90. BMC
Genomics 13, 613.
Watanabe, M.F., Tsujimura, S., Oishi, S., Niki, T., Namikoshi, M., 2003. Isolation and identification of homoanatoxin-a from a toxic
strain of the cyanobacterium Raphidiopsis mediterranea Skuja isolated from Lake Biwa, Japan. Phycologia 42, 364369.
Williams, P.G., Yoshida, W.Y., Moore, R.E., Paul, V.J., 2002. Isolation and structure determination of obyanamide, a novel cytotoxic
cyclic depsipeptide from the marine cyanobacterium Lyngbya confervoides. J. Nat. Prod. 65, 2931.
Wood, S.A., Rasmussen, J.P., Holland, P.T., Campbell, R., Crowe, A.L.M., 2007. First report of the cyanotoxin anatoxin-a from
Aphanizomenon issatschenkoi (cyanobacteria). J. Phycol. 43, 356365.
Yilmaz, M., Foss, A.J., Selwood, A.I., Özen, M., Boundy, M., 2018. Paralytic shellfish toxin producing Aphanizomenon gracile strains
isolated from Lake Iznik, Turkey. Toxicon 148, 132142.
Yilmaz, M., Phlips, E.J., Szabo, N.J., Badylak, S., 2008. A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon
for cylindrospermopsin production. Toxicon 51, 1309.
Yunes, J.S., De La Rocha, S., Giroldo, D., Silveira, S.B. Da, Comin, R., Bicho, M.D.S., Melcher, S.S., Sant'Anna, C.L., Vieira, A.A.H.,
2009. Release of carbohydrates and proteins by a subtropical strain of Raphidiopsis brookii (cyanobacteria) able to produce
saxitoxin at three nitrate concentrations. J. Phycol. 45, 585591.
... The most commonly cited cyanotoxins include microcystins (and their variants), cylindrospermopsin, and anatoxin-a. These cyanotoxins are often associated with various genus and/or species of the cyanobacteria, allowing for broad generalizations related to exposure potential [2]. ...
... Anatoxin-a is a neuroactive compound, that represents an acute exposure profile. Anatoxin-a is most commonly associated with bloom-forming cyanobacteria (BFC's) in the Order Nostocales [2] [3] including Dolichospermum flos-aquae [4] [5] [6] and Cuspidothrix issatschenkoi [7] [8] [9] [10]. Among the cyanobacteria the single celled picocyanobacteria (Order Synechococcales) are commonly found in both marine and freshwater systems [11]- [16]. ...
... MCs are extensively studied cyanotoxin that is produced by an array of cyanobacteria, including Dolichospermum, Microcystis, Planktothrix, Oscillatoria, and Anabaenopsis (Bernard et al., 2017;Chapman and Foss, 2019). So far, more than 300 variants of it have been characterized (Bouaïcha et al., 2019;Jones et al., 2021). ...
... CYN is a cyclic guanidine alkaloid. The species producing this toxin belong to certain cyanobacterial genera including Raphidiopsis, Aphanizomenon, Dolichospermum, and Lyngbya (Chapman and Foss, 2019). It primarily shows its toxicity on liver, kidney, heart, spleen, etc. ...
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Cyanobacterial harmful algal blooms (CHABs) are increasing at an alarming rate in different water bodies worldwide. In India, CHAB events in water bodies such as Dal Lake have been sporadically reported with no study done to characterize the cyanobacterial species and their associated toxins. We hypothesized that this Lake is contaminated with toxic cyanobacterial species with the possibility of the presence of cyanotoxin biosynthetic genes. We, therefore, used some of the molecular tools such as 16S ribosomal DNA, PCR, and phylogenetic analysis to explore cyanobacterial species and their associated toxins. A 3-year (2018–2020) survey was conducted at three different sampling sites of Dal Lake namely, Grand Palace Gath (S1), Nigeen basin (S2), and Gagribal basin (S3). Two strains of Dolichospermum sp. AE01 and AE02 (S3 and S1 site) and one strain of Microcystis sp. AE03 (S2 site) was isolated, cultured, and characterized phylogenetically by 16S ribosomal DNA sequencing. The presence of cyanotoxin genes from the isolates was evaluated by PCR of microcystins (mcyB), anatoxins (anaC), and cylindrospermopsins (pks) biosynthesis genes. Results revealed the presence of both mcyB and pks gene in Microcystis sp. AE03, and only anaC gene in Dolichospermum sp. AE02 strain. However, Dolichospermum sp. AE01 strain was not found to harbor any such genes. Our findings, for the first time, reported the coexistence of pks and mcyB in a Microcystis AE03 strain. This study has opened a new door to further characterize the unexplored cyanobacterial species, their associated cyanotoxin biosynthetic genes, and the intervention of high-end proteomic techniques to characterize the cyanotoxins.
... In general, cyanobacterial populations can be described using photosynthetic accessory pigments and size-structure analysis [1] [3] to provide detailed descriptions of these populations. The picocyanobacteria can produce secondary metabolites including microcystin (MC) and its variants and B-Methylamino-L-alanine (BMAA) [4] [5]. Recent genomic [6] and 16s metabarcoding [7] analysis has confirmed that commonly found picocyanobacteria (Order Synechococcales) can produce anatoxin-a. ...
... This toxin was isolated from Oscillatoria spp., benthic Microcoleus spp., Raphidiopsis spp., and Cylindrospermum spp. (Chapman and Foss 2020). Homoanatoxin-a differs from ATX-a by a single methyl group and the two alkaloid groups that share almost identical toxicological properties. ...
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Cyanobacterial harmful algal blooms (CHABs) are a global environmental concern that encompasses public health issues, water availability, and water quality owing to the production of various secondary metabolites (SMs), including cyanotox-ins in freshwater, brackish water, and marine ecosystems. The frequency, extent, magnitude, and duration of CHABs are increasing globally. Cyanobacterial species traits and changing environmental conditions, including anthropogenic pressure , eutrophication, and global climate change, together allow cyanobacteria to thrive. The cyanotoxins include a diverse range of low molecular weight compounds with varying biochemical properties and modes of action. With the application of modern molecular biology techniques, many important aspects of cyanobacteria are being elucidated including, aspects of their diversity, gene-environment interactions, and genes that express cyanotoxins. The toxicological, environmental, and economic impacts of CHABs strongly advocate the need for continuing, extensive efforts to monitor cyanobacterial growth and to understand the mechanisms regulating species composition and cyanotoxin biosynthesis. In this review, we critically examined the genomic organization of some cyanobacterial species that lead to the production of cyanotoxins and their characteristic properties discovered to date.
... produces microcystin in all 3 reservoirs, and Sphaerospermum in Little Dixie (Table 4). The diazotroph Aphanizomenon was dominant in DiSalvo, and while not known to produce microcystin, it does produce the cyanotoxin cylindrospermopsin and the T&O compound geosmin (Chapman and Foss 2019). The increase in cyanobacterial biovolume (with the exception of DiSalvo), presence of PTOX, and increase in microcystin (Table 3). ...
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Landscape-level analyses based on land cover, morphology, and hydrology account for most of the cross-system variation in pelagic nutrients and suspended solids in Missouri reservoirs. They are based on geometric means, which reduce the influence of extreme temporal variation measured in individual reservoirs. This analysis of 3 conservation reservoirs, managed to benefit recreational fisheries, details how internal processes can alter nutrients, chlorophyll, mineral turbidity, and transparency in long-term (21-42 year) datasets, which contribute to temporal variation. Management practices include the addition of grass carp and herbicides to control nuisance macrophytes and shoreline stabilization with rock and water willow. Among these reservoirs, there is strong evidence that macrophyte removal can increase pelagic nutrients by >90%, resulting in a switch to plankton-dominated conditions (alternative states). In one case, eradication of aquatic vegetation increased mineral turbidity by >60%, which was reversed by reestablishing macrophytes and stabilizing the shoreline. This temporal series supports the modifications of phytoplankton-nutrient relations by mineral turbidity shown in statewide analyses. Collectively, the long-term data show a significant increase in cyanobacteria biovolume and cyanotoxins, with maximum microcystin concentrations increasing as much as 20 times. Actively flipping lakes to plankton-dominated systems via fisheries management and shoreline stabilization practices has negative impacts on overall water quality, with implications for human and wildlife health. ARTICLE HISTORY
... For example, both cryptophytes and dinoflagellates have 2 flagella, are known to participate in diel vertical migrations to take advantage of both the nutrient-rich hypolimnion and light-replete surface waters, and can supplement metabolic requirements with mixotrophy (Raven and Richardson, 1984;Lee, 2008). We classified phytoplankton by the following 6 taxonomic groups: (1) potentially toxigenic cyanophyta (Chapman and Foss, 2019), (2) non-toxin producing cyanophyta, (3) chlorophyta, (4) euglenophyta, (5) cryptophyta and dinoflagellates, and (6) chrysophyta, including chrysophytes, bacillariophyta, ochrophytes, and haptophytes (Supplementary Table 3). ...
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Cyanobacterial harmful algal blooms are one of the most prominent threats to water quality in freshwater ecosystems and are expected to become more common as the climate continues to change. While traditional strategies to manage algal blooms have focused on controlling nutrients, manipulating light as a way to reduce cyanobacteria is less frequently explored. Here, we propose the addition of glacial rock flour (GRF), a fine particulate that floats on the water's surface and remains suspended in the water column, to reduce light availability and in turn, phytoplankton biomass dominated by cyanobacteria. To determine if a sustained reduction in light could lower cyanobacteria biomass and microcystin concentrations, we applied GRF to large-scale (11 kL) mesocosm tanks for 9 consecutive days. Mesocosm tanks were amended by adding nitrogen and phosphorus to generate chlorophyte-and cyanophyte-dominated experimental tanks. To assess how the phytoplankton community was impacted in each tank, we measured photosynthetic irradiance parameters, the maximum quantum yield of photosystem II, gross primary productivity (GPP), phytoplankton biovolume, and phytoplankton community composition before and after the addition of GRF. GRF effectively reduced cyanophyte biovolume by 78% in the cyanophyte-dominated tanks, despite no significant change in total phytoplankton community biovolume. Cyanophytes were replaced by cryptophytes, which increased by 106% in the chlorophyte-dominated tanks and by 240% in the cyanophyte-dominated tanks. The change in photosynthetic irradiance parameters and GPP after the addition of GRF was not significantly different between any of the treatment or control groups, suggesting that either the cyanophytes will likely recover if light availability increases, or that the new cryptophyte-dominated community was well suited to a reduced light environment. Cyanobacterial blooms are expected to increase in frequency and magnitude as climate change progresses, but our study suggests that light manipulation may be a useful in-lake management strategy for controlling these blooms and warrants further investigation.
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Cyanobacterial blooms sometimes create secondary metabolites that can be transferred between trophic levels and accumulate in fish, but little is known about what time of year fish are most susceptible. Here, we examine microcystin in the muscle, liver, and kidney of bluegill and largemouth bass from an agricultural reservoir over 12 months. We identify which fish characteristics and water parameters best explain microcystin accumulation in fish tissues. Microcystin in bluegill was significantly higher than largemouth bass. In both species, microcystin was highest in livers (bluegill mean=57.6 ng g⁻¹, largemouth bass mean=71.8 ng g⁻¹ wet weight [ww]), then kidneys (bluegill mean=27.1, largemouth bass mean=22.7 ng g⁻¹ ww), followed by muscles (bluegill mean=7.6, largemouth bass mean=5.7 ng g⁻¹ ww). Adult bluegill feed on benthic macroinvertebrates and zooplankton, which may explain their higher microcystin concentrations compared to largemouth bass, which are primarily piscivorous. Harvest date emerged as the best predictor of microcystin in muscles and kidneys, with the highest concentrations occurring in April. Microcystin in water also emerged as a significant predictor, albeit much lower than harvest date, suggesting that low but persistent microcystin concentrations in water may result in accumulation of this cyanotoxin in fish. This study is the first to examine microcystin in fish from the North American Great Plains and one of only 5 studies that investigate microcystin in bluegill and largemouth bass. Additional investigation into the relationship between cyanobacteria and fish health is warranted, especially during spring when fish microcystin concentrations were highest.
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Microcystins (MCs) are potent hepatotoxins, and their presence in water bodies poses a threat to wildlife and human populations. Most of the available information refers to plankton, and much less is known about microcystins in other habitats. To broaden our understanding of the presence and environmental distribution of this group of toxins, we conducted extensive sampling throughout Spain, under a range of conditions and in distinct aquatic and terrestrial habitats. More than half of the tested strains were toxic; concentrations of the hepatotoxin were low compared with planktic communities, and the number of toxic variants identified in each sample of the Spanish strains ranged from 1–3. The presence of microcystins LF and LY (MC-LF and MC-LY) in the tested samples was significant, and ranged from 21.4% to 100% of the total microcystins per strain. These strains were only detected in cyanobacteria Oscillatoriales and Nostocales. We can report, for the first time, seven new species of microcystin producers in high mountain rivers and chasmoendolithic communities. This is the first report of these species in Geitlerinema and the confirmation of Anatoxin-a in Phormidium uncinatum. Our findings show that microcystins are widespread in all habitat types, including both aerophytic and endolithic peat bogs and that it is necessary to identify all the variants of microcystins in aquatic bodies as the commonest toxins sometimes represent a very low proportion of the total. © 2017 by the authors. Licensee MDPI, Basel, Switzerland. All rights reserved.
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In the present work, we attempted to characterize two isolates of Cylindrospermopsis raciborskii, LP1 and LP2, from Peri Lagoon, for their morphology, ecophysiology, and toxin profiles. The genetic identity of the isolates was confirmed by amplifying and sequencing 16S rRNA. The isolates showed different morphologies and significant differences in the length of trichomes. LP2 showed a trend for higher growth rates than LP1 at the different temperatures and N:P ratios. Both isolates showed low light requirements, but were able to tolerate irradiances of around 200 μmol photons m⁻² s⁻¹. LP2 showed higher concentrations of saxitoxin than LP1 and wider range of analogs, therefore being considered more toxic. These results support the hypothesis of ecotype selection for this species, which probably originated in response to environmental fluctuations in Peri Lagoon. Dominance during almost the entire year can be explained by the alternation of these ecotypes in the total biomass contribution according to their physiological advantages, contributing to the ecological success of this species.
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p>Seasonal blooms of cyanobacteria (CB) are a typical feature of Lake Alto Flumendosa (Sardinia, Italy). The waters of this lake are used for drinking water supply, for agricultural and industrial uses, and fish farming activities. Since cyanotoxins are not monitored in edible organisms, diet could be a relevant route of human exposure. CB also represent a threat for the health of wild and domestic animals that use lake water for beverage. Therefore, to characterize the CB community and assess the risk for human and animal population, CB dynamic, mcy B<sup>+</sup> fraction, and microcystins (MCs) concentration have been followed monthly for 18 months, in three stations. Results confirmed the presence of several toxigenic species. Planktothrix rubescens dominated between August 2011 and April 2012 (3.5×10<sup>6</sup> cells L<sup>-1</sup>), alternating with Woronichinia naegeliana (8×10<sup>6</sup> cells L<sup>-1</sup>) and Microcystis botrys (9×10<sup>5</sup> cells L<sup>-1</sup>). Dolichospermum planctonicum was always present at low densities (10<sup>4 </sup>cells L<sup>-1</sup>). MCs were detected, at values well below the 1 µg L<sup>-1</sup> threshold of WHO for drinking water. The molecular analysis of mcy B gene for P. rubescens indicated the presence of a persistent toxic population (average 0.45 mcy B/16S rDNA). Highly significant linear regressions were found between P. rubescens and the sum of the demethylated MC variants, and between M. botrys and the sum of MC-LR and MC-LA, also when co-occurring, suggesting that these two species were responsible for different MC patterns production. The regression lines indicated a quite stable MC cell quota. However, in some spotted samples very different values were obtained for both MC concentrations and cell quota (from 10-fold lower to 30-40-fold higher than the ‘average’) showing an unexpected significant variability in the rate of toxin production. The relatively low cell densities during the monitoring period is consistent with the low-to absent MC contamination level found in trout muscle; however, the analytical method was affected by low recovery, probably due to MC-protein binding. Our results show that, during the study period, no risk of exposure for the human and animal population occurred. However, the persistence of a complex CB community characterised by a significant toxic fraction suggests the need for periodic monitoring activity. Particularly, the hidden deep summer P. rubescens blooms, located where water is taken for drinking water supply, and M. botrys , able to produce the most toxic MC variants with high cell quota, should be kept under control. The documentation and interpretation of sudden changes in toxins concentrations deserve special attention. This is particularly relevant in proximity of fish farming plants and water catchment sites. </p
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Background Very few closed genomes of the cyanobacteria that commonly produce toxic blooms in lakes and reservoirs are available, limiting our understanding of the properties of these organisms. A new anatoxin-a-producing member of the Nostocaceae, Anabaena sp. WA102, was isolated from a freshwater lake in Washington State, USA, in 2013 and maintained in non-axenic culture. ResultsThe Anabaena sp. WA102 5.7 Mbp genome assembly has been closed with long-read, single-molecule sequencing and separately a draft genome assembly has been produced with short-read sequencing technology. The closed and draft genome assemblies are compared, showing a correlation between long repeats in the genome and the many gaps in the short-read assembly. Anabaena sp. WA102 encodes anatoxin-a biosynthetic genes, as does its close relative Anabaena sp. AL93 (also introduced in this study). These strains are distinguished by differences in the genes for light-harvesting phycobilins, with Anabaena sp. AL93 possessing a phycoerythrocyanin operon. Biologically relevant structural variants in the Anabaena sp. WA102 genome were detected only by long-read sequencing: a tandem triplication of the anaBCD promoter region in the anatoxin-a synthase gene cluster (not triplicated in Anabaena sp. AL93) and a 5-kbp deletion variant present in two-thirds of the population. The genome has a large number of mobile elements (160). Strikingly, there was no synteny with the genome of its nearest fully assembled relative, Anabaena sp. 90. Conclusion Structural and functional genome analyses indicate that Anabaena sp. WA102 has a flexible genome. Genome closure, which can be readily achieved with long-read sequencing, reveals large scale (e.g., gene order) and local structural features that should be considered in understanding genome evolution and function.
A new nodularin producing benthic cyanobacterium Iningainema pulvinus gen nov., sp nov. was isolated from a freshwater ambient spring wetland in tropical, north-eastern Australia and characterised using combined morphological and phylogenetic attributes. It formed conspicuous irregularly spherical to discoid, blue-green to olive-green cyanobacterial colonies across the substratum of shallow pools. Morphologically Iningainema is most similar to Scytonematopsis Kiseleva and Scytonema Agardh ex Bornet & Flahault. All three genera have isopolar filaments enveloped by a firm, often layered and coloured sheath; false branching is typically geminate, less commonly singly. Phylogenetic analyses using partial 16S rRNA sequences of three clones of Iningainema pulvinus strain ES0614 showed that it formed a well-supported monophyletic clade. All three clones were 99.7–99.9% similar, however they shared less than 93.9% nucleotide similarity with other cyanobacterial sequences including putatively related taxa within the Scytonemataceae. Amplification of a fragment of the ndaF gene involved in nodularin biosynthesis from Iningainema pulvinus confirmed that it has this genetic determinant. Consistent with these results, analysis of two extracts from strain ES0614 by HPLC–MS/MS confirmed the presence of nodularin at concentrations of 796 and 1096 μg g⁻¹ dry weight. This is the third genus of cyanobacteria shown to produce the cyanotoxin nodularin and the first report of nodularin synthesis from the cyanobacterial family Scytonemataceae. These new findings may have implications for the aquatic biota at Edgbaston Reserve, a spring complex which has been identified as a priority conservation area in the central Australian arid and semiarid zones, based on patterns of endemicity.