Application of first order rate kinetics to explain changes in bloom toxicity-the importance of understanding cell toxin quotas -- Journal of Oceanology and Limnology,2018,36(4):1063-1074

	Cite this paper:
	Philip T. ORR, Anusuya WILLIS, Michele A. BURFORD. Application of first order rate kinetics to explain changes in bloom toxicity-the importance of understanding cell toxin quotas[J]. Journal of Oceanology and Limnology, 2018, 36(4): 1063-1074

Application of first order rate kinetics to explain changes in bloom toxicity-the importance of understanding cell toxin quotas

Philip T. ORR, Anusuya WILLIS, Michele A. BURFORD

Australian Rivers Institute, Griffith University, 170 Kessels Rd, Nathan, Qld 4111, Australia

Abstract:

Cyanobacteria are oxygenic photosynthetic Gram-negative bacteria that can form potentially toxic blooms in eutrophic and slow flowing aquatic ecosystems. Bloom toxicity varies spatially and temporally, but understanding the mechanisms that drive these changes remains largely a mystery. Changes in bloom toxicity may result from changes in intracellular toxin pool sizes of cyanotoxins with differing molecular toxicities, and/or from changes in the cell concentrations of toxic and non-toxic cyanobacterial species or strains within bloom populations. We show here how first-order rate kinetics at the cellular level can be used to explain how environmental conditions drive changes in bloom toxicity at the ecological level. First order rate constants can be calculated for changes in cell concentration (μ_c:specific cell division rate) or the volumetric biomass concentration (μ_g:specific growth rate) between short time intervals throughout the cell cycle. Similar first order rate constants can be calculated for changes in nett volumetric cyanotoxin concentration (μ_tox:specific cyanotoxin production rate) over similar time intervals. How μ_c (or μ_g) covaries with μ_tox over the cell cycle shows conclusively when cyanotoxins are being produced and metabolised, and how the toxicity of cells change in response to environment stressors. When μ_tox/μ_c>1, cyanotoxin cell quotasincrease and individual cells become more toxic because the nett cyanotoxin production rate is higher than the cell division rate. When μ_tox/μ_c=1, cell cyanotoxin quotas remains fixed because the nett cyanotoxin production rate matches the cell division rate. When μ_tox/μ_c<1, the cyanotoxin cell quota decreases because either the nett cyanotoxin production rate is lower than the cell division rate, or metabolic breakdown and/or secretion of cyanotoxins is occurring. These fundamental equations describe cyanotoxin metabolism dynamics at the cellular level and provide the necessary physiological background to understand how environmental stressors drive changes in bloom toxicity.

Key words: cyanotoxin production dynamics|first order rate kinetics|cyanobacteria

Received: 2017-06-28 Revised:

Tools

PDF (844 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by Philip T. ORR

Articles by Anusuya WILLIS

Articles by Michele A. BURFORD

References:
Anderson D M, Kulis D M, Sullivan J J, Hall S, Lee C. 1990.Dynamics and physiology of saxitoxin production by the dinoflagellates Alexandrium spp. Marine Biol., 104(3):511-524, https://doi.org/10.1007/BF01314358.
Bishop C T, Anet E F, Gorham P R. 1959. Isolation and identification of the fast-death factor in Microcystis aeruginosa NRC-1. Can J Biochem Physiol., 37(3):453-471.
Botes D P, Tuinman A A, Wessels P L, Viljoen C C, Kruger H, Williams D H, Santikarn S, Smith R J, Hammond S J. 1984. The structure of cyanoginosin-LA, a cyclic heptapeptide toxin from the cyanobacterium Microcystis aeruginosa. J. Chem. Soc. Perkin Trans., 1:2 311-2 318, https://doi.org/10.1039/P19840002311.
Bourne D G, Jones G J, Blakeley R L, Jones A, Negri A P, Riddles P. 1996. Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Appl. Environ. Microbiol., 62(11):4 086-4 094.
Bowling L C, Baker P D. 1996. Major cyanobacterial bloom in the Barwon-Darling River, Australia in 1991, and underlying limnological conditions. Aust. J. Mar.Freshwat. Res., 47:643-657, https://doi.org/10.1071/MF9960643.
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, https://doi.org/10.1016/j.hal.2015.10.012.
Byth S. 1980a. Palm Island mystery disease. Med. J. Aust., 2(1):40-42.
Byth S. 1980b. Correction. Palm Island mystery disease. Med.J. Aust., 2(3):170-170.
Carmichael W W, Gorham P R. 1981. The mosaic nature of blooms of toxic cyanobacteria. In:Carmichael W W ed. The Water Environment, Algal Toxins and Health.Springer US, Plenum Press, New York. p.161-172, https://doi.org/10.1007/978-1-4613-3267-1_12.
Carneiro R L, dos Santos M E V, Pacheco A B F, Azevedo S M F O. 2009. Effects of light intensity and light quality on growth and circadian rhythm of saxitoxins production in Cylindrospermopsis raciborskii (Cyanobacteria). J.Plankton Res., 31:481-488, https://doi.org/10.1093/plankt/fbp006.
Carneiro R L, Pacheco F, Beatriz A, Azevedo F de O e, Maria S. 2013. Growth and saxitoxin production by Cylindrospermopsis raciborskii (cyanobacteria) correlate with water hardness. Marine Drugs, 11(8):2 949-2 963, https://doi.org/10.3390/md11082949.
Castro D, Vera D, Lagos N, Garcıa C, Vásquez M. 2004. The effect of temperature on growth and production of paralytic shellfish poisoning toxins by the cyanobacterium Cylindrospermopsis raciborskii C10. Toxicon, 44:483-489, https://doi.org/10.1016/j.toxicon.2004.06.005.
Davis T W, Orr P T, Boyer G L, Burford M A. 2014.Investigating the production and release of cylindrospermopsin and deoxy-cylindrospermopsin by Cylindrospermopsis raciborskii over a natural growth cycle. Harmful Algae, 31:18-25, https://doi.org/10.1016/j.hal.2013.09.007.
Deem A W, Thorp F. 1939. Toxic algae in Colorado. J. Am. Vet.Med. Assoc., 95:542-544. Francis G. 1878. Poisonous Australian Lake. Nature, 18:11-12.
Gorham P R. 1964. Toxic Algae. In:Ed Jackson D F. Algae and Man. p.307-336. Springer US, Plennum Press, New York, https://doi.org/10.1007/978-1-4684-1719-7_15.
Gorham P. 1960. Toxic waterblooms of blue-green algae. The Can. Vet. J., 1(6):235-245.
Hawkins P R, Putt E, Falconer I, Humpage A. 2001.Phenotypical variation in a toxic strain of the phytoplankter, Cylindrospermopsis raciborskii(Nostocales, cyanophyceae) during batch culture.Environ. Toxicol., 16(6):460-467, https://doi.org/10.1002/tox.10005.
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. Appl.Environ. Microbiol., 50(5):1 292-1 295.
Humpage A R, Rositano J, Bretag A H, Brown R, Baker P D, Nicholson B C, Steffensen D A. 1994. Paralytic shellfish poisons from Australian cyanobacterial blooms.Australian Journal of Marine and Freshwater Research, 45(5):761-771, https://doi.org/10.1071/MF9940761.
Jähnichen S, Ihle T, Petzoldt T. 2008. Variability of microcystin cell quota:A small model explains dynamics and equilibria. Limnologica, 38:339-349, https://doi.org/10.1016/j.limno.2008.05.003
Jochimsen E M, Carmichael W W, An J, Cardo D M, Cookson S T, Holmes C E M, Antunes M B, Filho D A de M, Lyra T M, Barreto V S T, Azevedo S M F O, Jarvis W R. 1998.Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N. Engl J. Med., 338:873-878, https://doi.org/10.1056/NEJM199803263381304.
Kiviranta J, Sivonen K, Lahti K, Luukkainen R, Niemelä S I. 1991. Production and biodegradation of cyanobacterial toxins-a laboratory study. Arch. Hydrobiol., 121(3):281-294.
Kuiper-Goodman T, Falconer I, Fitzgerald J. 1999. Human Health Aspects. In:Ed Chorus I, Bartram J eds. Toxic cyanobacteria in water:A guide to their public health consequences and management, p.133-153. E and FN Spon on behalf of the World Health Organization.
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, https://doi.org/10.1016/S0041-0101(99)00080-X.
Lehtimäki J, Sivonen K, Luukkainen R, Niemelä S I. 1994.The effects of incubation time, temperature, light, salinity, and phosphorus on growth and hepatotoxin production by Nodularia strains. Arch. Hydrobiol., 130(3):269-282.
Long B M, Jones G J, Orr P T. 2001. Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Appl. Environ. Microbiol., 67(1):278-283, https://doi.org/10.1128/AEM.67.1.278-283.2001.
Lukač M, Aegerter R. 1993. Influence of trace metals on growth and toxin production of Microcystis aeruginosa.Toxicon, 31(3):293-305, https://doi.org/10.1016/0041-0101(93)90147-B.
Lyck S. 2004. Simultaneous changes in cell quotas of microcystin, chlorophyll a, protein and carbohydrate during different growth phases of a batch culture experiment with Microcystis aeruginosa. J. Plankt. Res., 26(7):727-736, https://doi.org/10.1093/plankt/fbh071.
McLeod J A, Bondar G F. 1952. A case of suspected algal poisoning in Manitoba. Can. J. Public Health, 43:347-350.
Negri A P, Jones G J, Blackburn S I, Oshima Y, Onodera H. 1997. Effect of culture and bloom development and of sample storage on paralytic shellfish poisons in the cyanobacterium Anabaena circinalis. J. Phycol., 33:26-35.
Negri A P, Jones G J, Hindmarsh M. 1995. Sheep mortality associated with paralytic shellfish poisons from the cyanobacterium Anabaena circinalis. Toxicon, 33(10):1 321-1 329, https://doi.org/10.1016/0041-0101(95)00068-W.
Neumann C, Bain P, Shaw G. 2007. Studies of the comparative in vitro toxicology of the cyanobacterial metabolite deoxycylindrospermopsin. J. Toxicol. Environ. Health, Part A, 70:1 679-1 686, https://doi.org/10.1080/15287390701434869.
NHMRC and NRMMC. 2011. Australian Drinking Water Guidelines. Paper 6. National Water Quality Management Strategy. National Health and Medical Research Council, National Resource Management Ministerial Council, Commonwealth of Australia, Canberra. ISBN Online:1864965118. https://www.nhmrc.gov.au/_files_nhmrc/file/publications/nhmrc_adwg_6_version_3.3_2.pdf.
Norris R, Eaglesham G, Pierens G, Shaw G, Smith M, Chiswell R, SeawrightA, Moore M. 1999. Deoxycylindrospermopsin, an analogue of cylindrospermopsin from Cylindrospermopsis raciborskii. Environ. Toxicol., 14:163-165, https://doi.org/10.1002/(SICI)1522-7278(199902)14:1<163::AID-TOX21>3.0.CO;2-V.
Orr P T, Jones G J, Hamilton G R. 2004. Removal of saxitoxins from drinking water by granular activated carbon, ozone and hydrogen peroxide-implications for compliance with the Australian drinking water guidelines. Wat. Res., 38(20):4 455-4 461, https://doi.org/10.1016/j.watres.2004.08.024.
Orr P T, Jones G J. 1998. Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnol. Oceanogr., 43(7):1 604-1 614, https://doi.org/10.4319/lo.1998.43.7.1604.
Pierangelini M, Sinha R, Willis A, Burford M A, Orr P T, Beardall J, Neilan B A. 2015. Constitutive cylindrospermopsin pool size in Cylindrospermopsis raciborskii under different light and CO₂ partial pressure conditions. Appl. Environ. Microbiol., 81(9):3 069-3 076, https://doi.org/10.1128/AEM.03556-14.
Pierangelini M, Stojkovic S, Orr P T, Beardall, J. 2014.Elevated CO₂ causes changes in the photosynthetic apparatus of a toxic cyanobacterium, Cylindrospermopsis raciborskii. J. Plant Physiol., 171(12):1 091-1 098, https://doi.org/10.1016/j.jplph.2014.04.003.
Rapala J K, Sivonen K, Lyra C, Niemelä S I. 1997. Variations in microcystins, cyanobacterial hepatotoxins, in Anabaena sp. as a function of growth stimuli. Appl. Environ.Microbiol., 63:2 206-2 212.
Rose E T. 1953. Toxic algae in Iowa lakes. Proc. Iowa. Acad.Sci., 60:738-745.
Sivonen K, Kononen K, Carmichael W W, Dahlem A M, Rinehart K L, Kiviranta J, Niemelä S I. 1989. Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and structure of the toxin. Appl. Environ.Microbiol., 55(8):1 990-1 995.
Sivonen K. 1990. Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Appl.Environ. Microbiol., 56(9):2 658-2 666.
Stewart I, Wickramasinghe W, Eaglesham G, Carroll A, McGregor G, Carter S, Shaw G, Seawright A. 2017. The acute toxicity of deoxy-cylindrospermopsin in Balb/c mice. 10^th International Conference on Cyanobacteria.Wuhan, China. October 2017.
Testé V, Briand J-F, Nicholson B C, Puiseux-Dao S. 2003.Comparison of changes in toxicity during growth of Anabaena circinalis (cyanobacteria) determined by mouse neuroblastoma bioassay and HPLC. J. Appl.Phycol., 14:399-407, https://doi.org/10.1023/A:1022101320029.
Utkilen H, Gjølme N. 1992. Toxin production by Microcystis aeruginosa as a function of light in continuous cultures and its ecological significance. Appl. Environ. Microbiol., 58(4):1 321-1 325.
van der Westhuizen A J, Eloff J N. 1983. Effect of culture age and pH of culture medium on the growth and toxicity of the blue-green alga Microcystis aeruginosa. Z.Pflanzenphysiol. Bd., 110(S):157-163.
Watanabe M F, Oishi S. 1985. Effects of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa)under culture conditions. Appl. Environ. Microbiol., 49(5):1 342-1 344.
Wicks R J, Thiel P G. 1990. Environmental factors affecting the production of peptide toxins in floating scums of the cyanobacterium Microcystis aeruginosa in a hypertrophic African reservoir. Environ. Sci. Technol., 24(9):1 413-1 418, https://doi.org/10.1021/es00079a017.
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) Seenaya et Subba Raju). Harmful Algae, 47:27-34, https://doi.org/10.1016/j.hal.2015.05.011.
Willis A, Chuang A W, Woodhouse J N, Neilan B A, Burford M A. 2016. Intraspecific variation in growth, morphology and toxin quotas for the cyanobacterium Cylindrospermopsis raciborskii. Toxicon, 119:307-310, https://doi.org/10.1016/j.toxicon.2016.07.005.
Wood S A, Borges H, Puddick J, Biessy L, Atalah J, Hawes I, Dietrich D R, Hamilton D P. 2017b. Contrasting cyanobacterial communities and microcystin concentrations in summers with extreme weather events:insights into potential effects of climate change.Hydrobiol., 785:71-89, https://doi.org/10.1007/s10750-016-2904-6.
Wood S A, Puddick J, Fleming R, Heussner A H. 2017a.Detection of anatoxin-producing Phormidium in a New Zealand farm pond and an associated dog death. NZ J.Bot., 55(1):36-46, https://doi.org/10.1080/0028825X.2016.1231122.