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USGS Mendenhall Postdoctoral Research Fellowship Program

S32. Characterization of cyanobacteria that lead to Harmful Algal Blooms

Understanding cyanobacterial harmful algal blooms (cyanoHABs) requires reliable scientific information on the species present in a bloom, genetic information on their capacity to produce cyanotoxins and the environmental ques that cause a species to initiate the cyanotoxin synthesis process (Pearson and Neilan, 2008, Davis et al. 2009, Burford et al. 2014, Pacheco et. al. 2016, Rosen et al., 2017). Traditional methods for identifying cyanobacteria relied exclusively on morphological characteristics (Anagnostidis and Komárek 1985). The advent of genetic sequencing has led to a polyphasic approach that removes some of the ambiguity that is derived from overlapping morphological features (Zapomělová et al. 2009, Komárek et al. 2014, Komárek 2016). Combining proper taxonomic assignment of organisms with their genetic information and actual toxin production, provides the foundation for advancing the understand of cyanoHABs and their potential impact on society (ecosystems and humans).

The U.S. Geological Survey (USGS) is collaborating internally and with federal agencies, state agencies, universities, public utilities, and Tribes to collect as many cyanobacteria species forming blooms and potentially producing toxins. Live samples are shipped directly to our research laboratory where organisms are photographed, morphological features documented, and individual species are brought into culture for additional studies.

Exposure to cyanobacterial toxins, such as anatoxins, cylindrospermopsins, microcystins, nodularins, and saxitoxins can result in significant health risks and can lead to mammalian mortality or illness (Kuiper-Goodman et al. 1999; Carmichael, 2001; Pearson et al. 2010). Currently, the most commonly detected cyanotoxins are the microcystins that are non-ribosomal peptide or polyketide toxins and common cyclic peptide structure (Welker and von Dohren, 2006) which inhibit protein phosphatases in the liver (Rinehart et al. 1994). Although the genus Microcystis has members that are known to produce this compound (Neilan et al. 1999), phylogenically disparate organisms such as Planktothrix (Christiansen et al. 2003) and Dolichospermum (Rouhianen 2004) are also known to synthesize microcystins.

The cylindrospermopsins are alkaloids with guanidinium and sulfate groups, with hepatotoxic, nephrotoxic and cytological effects (Falconer et al. 1999, Runnegar et al. 2002). Known producers of this compound include Cylindrospermopsis raciborskii (Ohtani et al. 1992; Sinha et al. 2014), Chyrsosporum ovalisporum (Banker et al. 1997), Rhaphidiopsis curvata (Li et al. 2001), Anabaena (Spoof et al. 2006) and other genera. Loftin et al. (2016) found 7% of lakes surveyed had detection of cylindrospermopsin, although attributing this compound to any given organism in a bloom needs greater study. For example, in the summer of 2017 the network of samples acquired by the USGS algae laboratory in Orlando had many locations with the presence of a previously unidentified organism, tentatively identified as Umezakia, a known producer of cylindrospermopsin (Terao et al. 1994), but it is unknown if this organism was producing this compound or posed a risk to humans and wildlife.

The nodularins are cyclic peptides commonly associated with the genus Nodularia. Although Nodularia spumigena blooms in water bodies, such as the Great Salt Lake, it is unclear if other organisms are synthesizing nodularins, given their prevalence in 4% of the lakes assessed (Loftin et al. 2016).

Improving the knowledge base of cyanobacteria in a harmful algal bloom centers on 1) accurately characterizing the morphology of the bloom-forming organism(s) so they can be properly identified and quantified (Rosen et al. 2017) with traditional microscopic techniques; 2) isolate and culture the bloom-forming species to examine both their toxin production and for the genes needed for toxin production. Many of the less common bloom-forming species have not been examined for their ability to make toxins. It is important to characterize these organisms because blooms are constantly changing, and examples of unidentified organisms blooming have the potential to be harmful. Genetic analyses of the unknown organisms, and contributing these data to genetic repositories like GenBank, will increase the robustness of monitoring programs that are relying more frequently on genomic data. Genetic information also provides insight into the regulation toxin production (Neilan et al. 2013).

This Mendenhall Research Fellowship will provide an excellent opportunity for an early career researcher to work collaboratively with USGS scientists and agency managers to provide scientific information through microscopic identification, novel enumeration techniques and genetic approaches that will be the foundational information for decision making. A team of scientists working across disciplines are participating in this effort and there is substantial room for creative approaches by the Mendenhall Fellow to propose original research to understand and improve our knowledge of species and their potential to cause harm to humans and wildlife. The research is expected to result in widely-distributed visual database and publications of toxin-producing cyanobacteria species. The postdoctoral researcher’s contributions are expected to provide insight into the less common species found in blooms, contribute data to genetic repositories, and advance our understanding of cyanobacterial bloom dynamics.

References

Anagnostidis K and Komárek J. 1985. Modern approach to the classification system of Cyanophytes 1 – introduction. Algological Studies 38–39: 291–302.

Banker R, Carmeli S, Hadas O, Teltsch B, Porat R, Sukenik A. 1997. Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from lake Kinneret. Israel. Journal of Phycology 33:613–616.

Burford MA, Davis TW, Orr PT, Sinha R, Willis A, Neilan BA. 2014. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microbial Ecology 89:135–148.

Carmichael WW. 2001. Health effects of toxin-producing cyanobacteria: “The CyanoHAB” Human Ecology Risk Assessment 7:1393–1407.

Christiansen G, Fastner J, Erhard M, Börner T, Dittmann E. 2003. Microcystin biosynthesis in Planktothrix: genes, evolution, and manipulation. Journal Bacteriology 185:564-72.

Davis TW., Berry DL, Boyer G., Gobler CJ. 2009. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8:715–725.

Falconer IR, Hardy, SJ, Humpage AR, Froscio, SM, Tozer GJ, and Hawkins PR. 1999. Hepatic and renal toxicity of the blue-green alga (cyanobacterium) Cylindrospermopsis raciborskii in male Swiss albino mice. Environmental Toxicology 14:143-150

Komárek J, Kaštovský J, Mareš J, Johansen JR. 2014. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) using a polyphasic approach. Preslia 86:295–335.

Komárek J. 2016. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications, European Journal of Phycology 51:346-353

Kuiper-Goodman T, Falconer I, Fitzgerald J. 1999. Human Health Aspects. In: Chorus I., Bartram J., editors. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management.E & FN Spon Publishers; London, UK p. 36.

Li R, Carmichael WW, Brittain S, Eaglesham GK, Shaw GR, Liu Y, Watanabe MM: First report of the cyanotoxins cylindrospermopsin and deoxycylindrospermopsin from Raphidiopsis curvata (cyanobacteria). Journal of Phycology 2001, 37(6):1121–1126

Loftin, KA, Graham JL, Hilborn ED, Lehmann SC, Meyer MT, Dietze JE, Meyer, Griffith, CB. 2016. Cyanotoxins in inland lakes of the United States: Occurrence and potential recreational health risks in the EPA National Lakes Assessment 2007. Harmful Algae 56:77-90.

Neilan BA, Dittmann E, Rouhiainen L, Bass RA, Schaub V, Sivonen K, Borner T. 1999. Nonribosomal peptide synthesis and toxigenicity of cyanobacteria. Journal of Bacteriology 181:4089–4097

Neilan BA, Pearson LA, Muenchhoff J, Moffitt MC, Dittmann E. 2013. Environmental conditions that influence toxin biosynthesis in cyanobacteria.Environmental Microbiology15:1239–1253.

Ohtani C, Ikuko MRE, Runnegar M. 1992. Cylindrospermopsin: a potent hepatotoxin from the blue-green alga Cylindrospermopsis raciborskii. Journal American Chemical Society 114:7941–7942.

Pacheco ABF, Guedes IA, Azevedo SMFO. 2016. Is qPCR a Reliable Indicator of Cyanotoxin Risk in Freshwater? Botana LM, ed. Toxins 8:172-198.

Pearson LA and Neilan BA. 2008. The molecular genetics of cyanobacterial toxicity as a basis for monitoring water quality and public health risk. Current Opinion in Biotechnology 19: 281-288.

Pearson L, Mihali T, Moffitt M, Kellmann R, Neilan B. 2010. On the chemistry, toxicology and genetics of the cyanobacterial toxins, microcystin, nodularin, saxitoxin and cylindrospermopsin. Marine Drugs 8:1650-80.

Rinehart KL, Namikoshi M, Choi BW. 1994. Structure and biosynthesis of toxins from blue-green algae (cyanobacteria). Journal Applied Phycology 2:159-176

Rosen, BH, Davis, TW, Gobler, CJ, Kramer, BJ, and Loftin, KA. 2017. Cyanobacteria of the 2016 Lake Okeechobee Waterway harmful algal bloom: U.S. Geological Survey Open-File Report 2017–1054, 34 p.

Rouhiainen L, Vakkilainen T, Siemer BL, Buikema W, Haselkorn R, Sivonen K. 2004. Genes coding for hepatotoxic heptapeptides (microcystins) in the cyanobacterium Anabaena strain 90. Applied Environmental Microbiology 70:686-92

Runnegar MT, Xie C, Snider BB, Wallace GA, Weinreb SM, Kuhlenkamp J. 2002. In Vitro Hepatotoxicity of the Cyanobacterial Alkaloid Cylindrospermopsin and Related Synthetic Analogues. Toxicological Sciences 67:81–87.

Sinha R, Leanne A Pearson LA, Davis TD, Muenchhoff J, Pratama R, Jex A, Burford MA, Neilan BA. 2014. Comparative genomics ofCylindrospermopsis raciborskiistrains with differential toxicities. BMC Genomics15:83-97.

Spoof L, Berg KA, Rapala J, Lahti K, Lepist L, Metcalf JS, Codd GA, Meriluoto J. 2006. First observation of cylindrospermopsin in Anabaena lapponica isolated from the boreal environment (Finland). Environmental Toxicology 21:552–560.

Terao K, Ohmori S, Igarashi K, Ohtani I, Watanabe MF, Harada KI, Ito E, Watanabe M: 1994. Electron microscopic studies on experimental poisoning in mice induced by cylindrospermopsin isolated from blue-green alga Umezakia natans. Toxicon 32(7):833–843.

Welker M and von Dohren H. 2006. Cyanobacterial peptides – nature’s own combinatorial biosynthesis. FEMS Microbiology Review 30:530-563.

Zapomělová E, Jezberová J, Hrouzek, P, Hisem, D., KomárkováJ. 2009. Polyphasic Characterization of three strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (Cyanobacteria) and their reclassification to Sphaerospermum Gen. Nov. (incl. Anabaena kisseleviana). Journal of Phycology 45:1363-1373.

Proposed Duty Station: Orlando, FL.

Areas of PhD: Phycology, microbial genetics, phytoplankton culturing, biology (candidates holding a Ph.D. in other disciplines, but with extensive knowledge and skills relevant to the Research Opportunity may be considered).

Qualifications: Applicants must meet one of the following qualifications: Research Biologist; Research Ecologist; Research Microbiologist. (This type of research is performed by those who have backgrounds for the occupations stated above. However, other titles may be applicable depending on the applicant's background, education, and research proposal. The final classification of the position will be made by the Human Resources specialist.)

Research Advisor(s): Barry Rosen, (407) 738-0669, brosen@usgs.gov.

Human Resources Office Contact: Diana Panchal, 703-648-7464, dpanchal@usgs.gov


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U.S. Department of the Interior, U.S. Geological Survey
URL: http://geology.usgs.gov/postdoc/opps/2019/S32 Rosen.htm
Direct inquiries to Cara A. Campbell at ccampbell@usgs.gov
Maintained by: Mendenhall Research Fellowship Program Web Team
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