Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, <i>Cylindrospermopsis raciborskii</i> -- Journal of Oceanology and Limnology,2018,36(4):1032-1039

	Cite this paper:
	Michele A. BURFORD, Anusuya WILLIS, Ann CHUANG, Xiao MAN, Philip T. ORR. Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii[J]. Journal of Oceanology and Limnology, 2018, 36(4): 1032-1039

Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii

Michele A. BURFORD, Anusuya WILLIS, Ann CHUANG, Xiao MAN, Philip T. ORR

Australian Rivers Institute, Griffith University, Australia

Abstract:

The harmful cyanobacterium Cylindrospermopsis raciborskii is a widespread species increasingly being recorded in freshwater systems around the world. Studies have demonstrated some key attributes of this species which may explain its global dominance. It has a high level of flexibility with respect to light and nutrients, being capable of growth under low and variable light conditions. However, it is the strategy with respect to nutrient utilization that has received more attention. Unlike many bloom forming species, the dominance of this species is not simply linked to higher nutrient loads. In fact it appears that it is more competitive when phosphorus and nitrogen availability is low and/or variable. An important component of this flexibility appears to be the result of within-population strain variability in responses to nutrients, as well as key physiological adaptations. Strain variability also appears to have an effect on the population-level cell quota of toxins, specifically cylindrospermopsins (CYNs). Field studies in Australia showed that populations had the highest proportion of toxic strains when dissolved inorganic phosphorus was added, resulting in stoichiometrically balanced nitrogen and phosphorus within the cells. These strategies are part of an arsenal of responses to environmental conditions, making it a challenging species to manage. However, our ability to improve bloom prediction will rely on a more detailed understanding of the complex physiology and ecology of this species.

Key words: nitrogen|phosphorus|cylindrospermopsins|strains

Received: 2017-06-21 Revised:

Tools

PDF (576 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by Michele A. BURFORD

Articles by Anusuya WILLIS

Articles by Ann CHUANG

Articles by Xiao MAN

Articles by Philip T. ORR

References:
Aguilera A, Aubriot L, Echenique R O, Salerno G L, Brena B M, Pírez M, Bonilla S. 2017. Synergistic effects of nutrients and light favor Nostocales over nonheterocystous cyanobacteria. Hydrobiologia, 794(1):241-255.
Amaral V, Bonilla S, Aubriot L. 2014. Growth optimization of the invasive cyanobacterium Cylindrospermopsis raciborskii in response to phosphate fluctuations.European Journal of Phycology, 49(1):134-141.
Ammar M, Comte K, Tran T D C, El Bour M. 2014. Initial growth phases of two bloom-forming cyanobacteria(Cylindrospermopsis raciborskii and Planktothrix agardhii) in monocultures and mixed cultures depending on light and nutrient conditions. Annales de LimnologieInternational Journal of Limnology, 50(3):231-240.
Antunes J T, Leão P N, Vasconcelos V M. 2015.Cylindrospermopsis raciborskii:review of the distribution, phylogeography, and ecophysiology of a global invasive species. Frontiers in Microbiology, 6:473.
Bai F, Liu R, Yang Y J, Ran X F, Shi J Q, Wu Z X. 2014.Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium,Cylindrospermopsis raciborskii. Harmful Algae, 39:112-120.
Bonilla S, Aubriot L, Soares M C S, González-Piana M, Fabre A, Huszar V L M, Lürling M, Antoniades D, Padisák J, Kruk C. 2012. What drives the distribution of the bloomforming cyanobacteria Planktothrix agardhii and Cylindrospermopsis raciborskii? FEMS Microbiology Ecology, 79(3):594-607.
Burford M A, Beardall J, Willis A, Orr P T, Magalhaes V F, Rangel L M, Azevedo S M F O E, Neilan B A. 2016.Understanding the winning strategies used by the bloomforming cyanobacterium Cylindrospermopsis raciborskii.Harmful Algae, 54:44-53.
Burford M A, Davis T W, Orr P T, Sinha R, Willis A, Neilan B A. 2014. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium Cylindrospermopsis raciborskii. FEMS Microbiology Ecology, 89(1):135-148.
Burford M A, McNeale K L, McKenzie-Smith F J. 2006. The role of nitrogen in promoting toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Freshwater Biology, 51(11):2 143-2 153.
Byth S. 1980. Palm Island mystery disease. The Medical Journal of Australia, 2(1):40, 42.
Chislock M F, Sharp K L, Wilson A. 2014. Cylindrospermopsis raciborskii dominates under very low and high nitrogento-phosphorus ratios. Water Research, 49:207-214.
Dolman A M, Rücker J, Pick F R, Fastner J, Rohlack T, Mischke U, Wiedner C. 2012. Cyanobacteria and cyanotoxins:the influence of nitrogen versus phosphorus.PLoS One, 7(6):e38757.
Droop M R. 1983. 25 years of algal growth kinetics:a personal view. Botanica Marina, 26(3):99-112.
Falkner G, Wagner F, Small J V, Falkner R. 1995. Influence of fluctuating phosphate supply on the regulation of phosphate uptake by the blue-green alga Anacystzs nidulans. Journal of Phycology, 31(5):745-753.
Figueredo C C, Giani A, Bird D F. 2007. Does allelopathy contribute to Cylindrospermopsis raciborskii(Cyanobacteria) bloom occurrence and geographic expansion? Journal of Phycology, 43(2):256-265.
Glibert P M, Allen J I, Bouwman A F, Brown C W, Flynn K J, Lewitus A J, Madden C J. 2010. Modeling of HABs and eutrophication:status, advances, challenges. Journal of Marine Systems, 83(3-4):262-275.
Glibert P M, Burford M A. 2017. Globally changing nutrient loads and harmful algal blooms:recent advances, new paradigms, and continuing challenges. Oceanography, 30(1):58-69.
Gobler C J, Burkholder J M, Davis T W, Harke M J, Johengen T, Stow C A, Van de Waal D B. 2016. The dual role of nitrogen supply in controlling the growth and toxicity of cyanobacterial blooms. Harmful Algae, 54:87-97.
Hawkins P R, Runnegar M T C, Jackson A R B, Falconer I R. 1985. Severe hepatotoxicity caused by the tropical cyanobacterium (blue-green alga) Cylindrospermopsis raciborskii (Woloszynska) Seenaya and Subba Raju isolated from a domestic water supply reservoir. Applied and Environmental Microbiology, 50(5):1 292-1 295.
Hong Y, Burford M A, Ralph P J, Doblin M A. 2015. Subtropical zooplankton assemblage promotes the harmful cyanobacterium Cylindrospermopsis raciborskii in a mesocosm experiment. Journal of Plankton Research, 37(1):90-101.
Hong Y, Burford M A, Ralph P J, Udy J W, Doblin M A. 2013.The cyanobacterium Cylindrospermopsis raciborskii is facilitated by copepod selective grazing. Harmful Algae, 29:14-21.
Isvánovics V, Shafik H M, Présing M A, Juhos S. 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology, 43(2):257-275.
Kenesi G, Shafik H M, Kovács A W, Herodek S, Présing M. 2009. Effect of nitrogen forms on growth, cell composition and N₂ fixation of Cylindrospermopsis raciborskii in phosphorus-limited chemostat cultures. Hydrobiologica, 623(1):191-202.
Kokociński M, Soininen J. 2012. Environmental factors related to the occurrence of Cylindrospermopsis raciborskii(Nostocales, Cyanophyta) at the north-eastern limit of its geographical range. European Journal of Phycology, 47(1):12-21.
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(10):1 359-1 373.
Lakeman M B, von Dassow P, Cattolico R A. 2009. The strain concept in phytoplankton ecology. Harmful Algae, 8(5):746-758.
Li R, Carmichael W W, Brittain S, Eaglesham G K, Shaw G R, Mahakhant A, Noparatnaraporn N, Yongmanitchai W, Kaya K, Watanabe M M. 2001. Isolation and identification of the cyanotoxin cylindrospermopsin and deoxycylindrospermopsin from a Thailand strain of Cylindrospermopsis raciborskii (Cyanobacteria). Toxicon, 39(7):973-980.
Marinho M M, Souza M B G, Lürling M. 2013. Light and phosphate competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa is strain dependent. Microbial Ecology, 66(3):479-488.
Moisander P H, Cheshire L A, Braddy J, Calandrino E S, Hoffman M, Piehler M F, Paerl H W. 2012. Facultative diazotrophy increases Cylindrospermopsis raciborskii competitiveness under fluctuating nitrogen availability.FEMS Microbiology Ecology, 79(3):800-811.
Monod J. 1942. Recherches sur la Croissance des Cultures Bactériennes. Herman, Paris, France. p.1-211.
Muhid P, Davis T W, Bunn S E, Burford M A. 2013. Effects of inorganic nutrients in recycled water on freshwater phytoplankton biomass and composition. Water Research, 47(1):384-394.
Neilan B A, Saker M L, Fastner J, Törökné A, Burns B P. 2003.Phylogeography of the invasive cyanobacterium Cylindrospermopsis raciborskii. Molecular Ecology, 12(1):133-140.
Oliver R L, Hamilton D P, Brookes J, Ganf G G. 2012.Physiology, blooms and prediction of planktonic cyanobacteria cyanobacteria. In:Whitton B A ed. Ecology of Cyanobacteria Ⅱ:Their Diversity in Space and Time.Springer, Dordrecht, Netherlands. p.155-194.
Padisák J. 1997. Cylindrospermopsis raciborskii(Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium:worldwide distribution and review of its ecology. Archiv für Hydrobiologie, 107(4):563-593.
Plominsky Á M, Delherbe N, Mandakovic D, Riquelme B, González K, Bergman B, Mariscal V, Vásquez M. 2015.Intercellular transfer along the trichomes of the invasive terminal heterocyst forming cyanobacterium Cylindrospermopsis raciborskii CS-505. FEMS Microbiology Letters, 362(5):fnu009.
Plominsky Á M, Larsson J, Bergman B, Delherbe N, Osses I, Vásquez M. 2013. Dinitrogen fixation is restricted to the terminal heterocysts in the invasive cyanobacterium Cylindrospermopsis raciborskii CS-505. PLoS One, 8(2):e51682.
Posselt A J, Burford M A, Shaw G. 2009. Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Journal of Phycology, 45(3):540-546.
Prentice M J, O'Brien K R, Hamilton D P, Burford M A. 2015.High-and low-affinity phosphate uptake and its effect on phytoplankton dominance in a phosphate-depauperate lake. Aquatic Microbial Ecology, 75(2):139-153.
Redfield A C. 1958. The biological control of chemical factors in the environment. American Scientist, 46(3):205-222.
Richie R J, Trautman D A, Larkum A W D. 2001. Phosphate limited cultures of the cyanobacterium Synechococcus are capable of very rapid, opportunistic uptake of phosphate.New Phytologist, 152(2):189-201.
Rzymski P, Poniedziałek B, Kokociński M, Jurczak T, Lipski D, Wiktorowicz K. 2014. Interspecific allelopathy in cyanobacteria:cylindrospermopsin and Cylindrospermopsis raciborskii, effect on the growth and metabolism of Microcystis aeruginosa. Harmful Algae, 35:1-8.
Saker M L, Neilan B A. 2001. Varied diazotrophies, morphologies, and toxicities of genetically similar isolates of Cylindrospermopsis raciborskii (Nostocales, Cyanophyceae) from Northern Australia. Applied and Environmental Microbiology, 67(4):1 839-1 845.
Sinha R, Pearson L, Davis T W, Muenchhoff J, Pratama R, Jex A, Burford M A, Neilan B. 2014. Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genomics, 15:83.
Soares M C S, Huszar V L M, Miranda M N, Mello M M, Roland F, Lürling M. 2013. Cyanobacterial dominance in Brazil:distribution and environmental preferences.Hydrobiologia, 717(1):1-12.
Stucken K, John U, Cembella A, Soto-Liebe K, Vásquez M. 2014. Impact of nitrogen sources on gene expression and toxin production in the diazotroph Cylindrospermopsis raciborskii CS-505 and non-diazotroph Raphidiopsis brookii D9. Toxins, 6(6):1 896-1 915.
Willis A, Adams M P, Chuang A W, Orr P T, O'Brien K R, Burford M A. 2015. Constitutive toxin production under various nitrogen and phosphorus regimes of three ecotypes of Cylindrospermopsis raciborskii ((Wołoszyńska) Seenayya et Subba Raju). Harmful Algae, 47:27-34.
Willis A, Chuang A W, Burford M A. 2016b. Nitrogen fixation by the reluctant diazotroph Cylindrospermopsis raciborskii (Cyanophyceae). Journal of Phycology, 52(5):854-862.
Willis A, Chuang A W, Woodhouse J N, Neilan B A, Burford M A. 2016a. Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium, Cylindrospermopsis raciborskii. Toxicon, 119:307-310.
Willis A, Posselt A J, Burford M A. 2017. Variations in carbonto-phosphorus ratios of two Australian strains of Cylindrospermopsis raciborskii. European Journal of Phycology, 52(3):303-310.
Wimmer K M, Strangman W K, Wright J L C. 2014. 7-Deoxydesulfo-cylindrospermopsin and 7-deoxy-desulfo-12-acetylcylindrospermopsin:two new cylindrospermopsin analogs isolated from a Thai strain of Cylindrospermopsis raciborskii. Harmful Algae, 37:203-206, https://doi.org/10.1016/j.hal.2014.06.006.
Wood S A, Stirling D J. 2003. First identification of the cylindrospermopsin-producing cyanobacterium Cylindrospermopsis raciborskii in New Zealand. New Zealand Journal of Marine and Freshwater Research, 37(4):821-828.
Wu Z X, Zeng B, Li R H, Song L R. 2012. Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae, 15:53-58.
Xiao M, Willis A, Burford M A. 2017. Differences in cyanobacterial strain responses to light and temperature reflect species plasticity. Harmful Algae, 62:84-93.