微囊藻毒素生物学功能的研究进展
Research Progress on Biological Function of Microcystins
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摘要: 在全球气候变化的大背景下,藻类水华暴发愈加频繁,产生的藻毒素对人类和动物的健康造成了严峻的威胁,其中以微囊藻毒素最为突出。阐明以微囊藻毒素为代表的藻毒素产生的原因无疑对水环境治理具有长远意义,然而微囊藻毒素的生物学功能至今尚不明确。微囊藻毒素的产生和多种环境条件相关,而微囊藻中也只有部分是产毒株系。尽管该毒素的毒理学靶点主要在人类和其他哺乳动物的蛋白磷酸酶,然而结合进化生物学和地质历史的证据可知,微囊藻毒素的出现比包括哺乳动物在内的后生动物的起源要早得多,因此微囊藻毒素并非藻类为了防御后生动物摄食而进化出来的,这引发了该毒素原本生物学功能的多年广泛研讨。本文综述了近年来关于微囊藻毒素生物学功能的新进展,并侧重在地质历史及当今全球气候变化背景下讨论该领域的研究意义。Abstract: Under the background of global climate change, algal bloom outbreaks are becoming more frequent, and the production of algal toxins pose a serious threat to human and animal health, among which microcystins are the most prominent. Elucidating the cause of algal toxins represented by microcystins is of great significance to water environment management in the long run. However, the biological function of microcystins is still unclear. The production of microcystins is related to a variety of environmental conditions, and only some of Microcystis strains are toxin-producing. Although the toxicological targets of the toxin are mainly protein phosphatases in human and mammalian, evolutionary biology and geological history suggest that microcystins emerged much earlier than the origin of metazoans, including mammals, and thus was not evolved by algae as a defense against metazoan feeding. This led to years of extensive researches on the original biological function of the toxins. This paper reviews recent advances in the biological function of microcystins and highlights their significance in the context of geological history and current global climate changes.
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Key words:
- microcystin /
- cyanobacterial bloom /
- biological function /
- global climate changes
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沈强, 胡菊香. 全球气候变化下的长江流域蓝藻水华暴发趋势[C]// 中国水利学会. 中国原水论坛专辑. 宁波: 中国水利学会, 2010: 359-360 谢平. 微囊藻毒素对人类健康影响相关研究的回顾[J]. 湖泊科学, 2009, 21(5): 603-613 Xie P. A review on the studies related to the effects of microcystins on human health[J]. Journal of Lake Sciences, 2009, 21(5): 603-613(in Chinese)
Fontanillo M, Köhn M. Microcystins: Synthesis and structure-activity relationship studies toward PP1 and PP2A[J]. Bioorganic & Medicinal Chemistry, 2018, 26(6): 1118-1126 Redouane E M, El Amrani Zerrifi S, El Khalloufi F, et al. Mode of action and fate of microcystins in the complex soil-plant ecosystems[J]. Chemosphere, 2019, 225: 270-281 靳红梅, 常志州. 微囊藻毒素对陆生植物的污染途径及累积研究进展[J]. 生态学报, 2013, 33(11): 3298-3310 Jin H M, Chang Z Z. The pollution way of microcystins and their bioaccumulation in terrestrial plants: A review[J]. Acta Ecologica Sinica, 2013, 33(11): 3298-3310(in Chinese)
胡智泉, 李敦海, 刘永定, 等. 微囊藻毒素对水生生物的生态毒理学研究进展[J]. 自然科学进展, 2006, 16(1): 14-20 Zhang S Y, Du X D, Liu H H, et al. The latest advances in the reproductive toxicity of microcystin-LR[J]. Environmental Research, 2021, 192: 110254 Ma Y, Liu H H, Du X D, et al. Advances in the toxicology research of microcystins based on Omics approaches[J]. Environment International, 2021, 154: 106661 Tamele I J, Vasconcelos V. Microcystin incidence in the drinking water of Mozambique: Challenges for public health protection[J]. Toxins, 2020, 12(6): 368 Hu L L, Shan K, Lin L Z, et al. Multi-year assessment of toxic genotypes and microcystin concentration in northern Lake Taihu, China[J]. Toxins, 2016, 8(1): 23 Yang Z, Kong F X, Zhang M. Groundwater contamination by microcystin from toxic cyanobacteria blooms in Lake Chaohu, China[J]. Environmental Monitoring and Assessment, 2016, 188(5): 280 Carmichael W W, Boyer G L. Health impacts from cyanobacteria harmful algae blooms: Implications for the North American Great Lakes[J]. Harmful Algae, 2016, 54: 194-212 Kalaitzidou M P, Nannou C I, Lambropoulou D A, et al. First report of detection of microcystins in farmed Mediterranean mussels Mytilus galloprovincialis in Thermaikos Gulf in Greece[J]. Journal of Biological Research, 2021, 28(1): 8 Koch M, Bowes G, Ross C, et al. Climate change and ocean acidification effects on seagrasses and marine macroalgae[J]. Global Change Biology, 2013, 19(1): 103-132 Guinotte J M, Fabry V J. Ocean acidification and its potential effects on marine ecosystems[J]. Annals of the New York Academy of Sciences, 2008, 1134: 320-342 Chiarenza A A, Farnsworth A, Mannion P D, et al. Asteroid impact, not volcanism, caused the end-Cretaceous dinosaur extinction[J]. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117(29): 17084-17093 Castle J W, Rodgers J H. Hypothesis for the role of toxin-producing algae in Phanerozoic mass extinctions based on evidence from the geologic record and modern environments[J]. Environmental Geosciences, 2011, 18(1): 58-60 Mata S A, Bottjer D J. Microbes and mass extinctions: Paleoenvironmental distribution of microbialites during times of biotic crisis[J]. Geobiology, 2012, 10(1): 3-24 Yao L, Aretz M, Chen J T, et al. Global microbial carbonate proliferation after the end-Devonian mass extinction: Mainly controlled by demise of skeletal bioconstructors[J]. Scientific Reports, 2016, 6(1): 1-9 Foster W J, Lehrmann D J, Yu M Y, et al. Facies selectivity of benthic invertebrates in a Permian/Triassic boundary microbialite succession: Implications for the “microbialite refuge” hypothesis[J]. Geobiology, 2019, 17(5): 523-535 Takahashi S, Yamakita S, Suzuki N. Natural assemblages of the conodont Clarkina in lowermost Triassic deep-sea black claystone from northeastern Japan, with probable soft-tissue impressions[J]. Palaeogeography, Palaeoclimatology, Palaeoecology, 2019, 524: 212-229 Gliwa J, Ghaderi A, Leda L, et al. Aras Valley (northwest Iran):High-resolution stratigraphy of a continuous central Tethyan Permian-Triassic boundary section[J]. Fossil Record, 2020, 23(1): 33-69 Sephton M, Amor K, Franchi I, et al. Carbon and nitrogen isotope disturbances and an end-Norian (Late Triassic) extinction event[J]. Geology, 2002, 30(12): 1119-1122 Duan X, Shi Z Q, Chen Y L, et al. Early Triassic Griesbachian microbial mounds in the Upper Yangtze Region, southwest China: Implications for biotic recovery from the latest Permian mass extinction[J]. PLoS One, 2018, 13(8): e0201012 Rantala A, Fewer D P, Hisbergues M, et al. Phylogenetic evidence for the early evolution of microcystin synthesis[J]. Proceedings of the National Academy of Sciences of the United States of America, 2004, 101(2): 568-573 Babica P, Bláha L, Maršálek B. Exploring the natural role of microcystins—A review of effects on photoautotrophic organisms[J]. Journal of Phycology, 2006, 42(1): 9-20 Kaplan A, Harel M, Kaplan-Levy R N, et al. The languages spoken in the water body (or the biological role of cyanobacterial toxins)[J]. Frontiers in Microbiology, 2012, 3: 138 Omidi A, Esterhuizen-Londt M, Pflugmacher S. Still challenging: The ecological function of the cyanobacterial toxin microcystin—What we know so far[J]. Toxin Reviews, 2018, 37(2): 87-105 Schatz D, Keren Y, Vardi A, et al. Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins[J]. Environmental Microbiology, 2007, 9(4): 965-970 Wang S Q, Yang S Y, Zuo J, et al. Simultaneous removal of the freshwater bloom-forming cyanobacterium microcystis and cyanotoxin microcystins via combined use of algicidal bacterial filtrate and the microcystin-degrading enzymatic agent, MlrA[J]. Microorganisms, 2021, 9(8): 1594 Waters M N, Brenner M, Curtis J H, et al. Harmful algal blooms and cyanotoxins in Lake Amatitlán, Guatemala, coincided with ancient Maya occupation in the watershed[J]. Proceedings of the National Academy of Sciences of the United States of America, 2021, 118(48): e2109919118 Zi J M, Pan X F, MacIsaac H J, et al. cyanobacteria blooms induce embryonic heart failure in an endangered fish species[J]. Aquatic Toxicology, 2018, 194: 78-85 Omidi A, Pflugmacher S, Kaplan A, et al. Reviewing interspecies interactions as a driving force affecting the community structure in lakes via cyanotoxins[J]. Microorganisms, 2021, 9(8): 1583 Cao Q, Steinman A D, Wan X, et al. Combined toxicity of microcystin-LR and copper on lettuce (Lactuca sativa L.)[J]. Chemosphere, 2018, 206: 474-482 Budzałek G, Śliwińska-Wilczewska S, Klin M, et al. Changes in growth, photosynthesis performance, pigments, and toxin contents of bloom-forming cyanobacteria after exposure to macroalgal allelochemicals[J]. Toxins, 2021, 13(8): 589 Brêda-Alves F, de Oliveira Fernandes V, Cordeiro-Araújo M K, et al. The combined effect of clethodim (herbicide) and nitrogen variation on allelopathic interactions between Microcystis aeruginosa and Raphidiopsis raciborskii[J]. Environmental Science and Pollution Research International, 2021, 28(9): 11528-11539 Chen G Y, Zheng Z H, Bai M X, et al. Chronic effects of microcystin-LR at environmental relevant concentrations on photosynthesis of Typha angustifolia Linn[J]. Ecotoxicology, 2020, 29(5): 514-523 Hernández-Zamora M, Santiago-Martínez E, Martínez-Jerónimo F. Toxigenic Microcystis aeruginosa (cyanobacteria) affects the population growth of two common green microalgae: Evidence of other allelopathic metabolites different to cyanotoxins[J]. Journal of Phycology, 2021, 57(5): 1530-1541 Yang J, Deng X R, Xian Q M, et al. Allelopathic effect of Microcystis aeruginosa on Microcystis wesenbergii: Microcystin-LR as a potential allelochemical[J]. Hydrobiologia, 2014, 727(1): 65-73 García-Espín L, Cantoral E A, Asencio A D, et al. Microcystins and cyanophyte extracts inhibit or promote the photosynthesis of fluvial algae. Ecological and management implications[J]. Ecotoxicology, 2017, 26(5): 658-666 Chia M A, Jankowiak J G, Kramer B J, et al. Succession and toxicity of Microcystis and Anabaena (Dolichospermum) blooms are controlled by nutrient-dependent allelopathic interactions[J]. Harmful Algae, 2018, 74: 67-77 González-Pleiter M, Cirés S, Wörmer L, et al. Ecotoxicity assessment of microcystins from freshwater samples using a bioluminescent cyanobacterial bioassay[J]. Chemosphere, 2020, 240: 124966 Wang N Y, Wang C. Effects of microcystin-LR on the tissue growth and physiological responses of the aquatic plant Iris pseudacorus L.[J]. Aquatic Toxicology, 2018, 200: 197-205 Lu N, Sun Y F, Wei J J, et al. Toxic Microcystis aeruginosa alters the resource allocation in Daphnia mitsukuri responding to fish predation cues[J]. Environmental Pollution, 2021, 278: 116918 Henao E, Rzymski P, Waters M N. A review on the study of cyanotoxins in paleolimnological research: Current knowledge and future needs[J]. Toxins, 2019, 12(1): 6 Schatz D, Keren Y, Vardi A, et al. Towards clarification of the biological role of microcystins, a family of cyanobacterial toxins[J]. Environmental Microbiology, 2007, 9(4): 965-970 Zilliges Y, Kehr J C, Meissner S, et al. The cyanobacterial hepatotoxin microcystin binds to proteins and increases the fitness of microcystis under oxidative stress conditions[J]. PLoS One, 2011, 6(3): e17615 Wang X, Wang P F, Wang C, et al. Relationship between photosynthetic capacity and microcystin production in toxic Microcystis aeruginosa under different iron regimes[J]. International Journal of Environmental Research and Public Health, 2018, 15(9): 1954 Walls J T, Wyatt K H, Doll J C, et al. Hot and toxic: Temperature regulates microcystin release from cyanobacteria[J]. The Science of the Total Environment, 2018, 610-611: 786-795 Xue Q J, Steinman A D, Xie L Q, et al. Seasonal variation and potential risk assessment of microcystins in the sediments of Lake Taihu, China[J]. Environmental Pollution, 2020, 259: 113884 Zhu C M, Zhang J Y, Nawaz M Z, et al. Seasonal succession and spatial distribution of bacterial community structure in a eutrophic freshwater Lake, Lake Taihu[J]. The Science of the Total Environment, 2019, 669: 29-40 Wang C B, Feng B, Tian C C, et al. Quantitative study on the survivability of Microcystis colonies in lake sediments[J]. Journal of Applied Phycology, 2018, 30(1): 495-506 Feng B, Wang C B, Wu X Q, et al. Involvement of microcystins, colony size and photosynthetic activity in the benthic recruitment of Microcystis[J]. Journal of Applied Phycology, 2019, 31(1): 223-233 Yu J, Zhu H, Shutes B, et al. Salt-alkalization may potentially promote Microcystis aeruginosa blooms and the production of microcystin-LR[J]. Environmental Pollution, 2022, 301: 118971 Trung B, Vollebregt M E, Lürling M. Warming and salt intrusion affect microcystin production in tropical bloom-forming Microcystis[J]. Toxins, 2022, 14(3): 214 Jia J M, Chen Q W, Wang M, et al. The production and release of microcystin related to phytoplankton biodiversity and water salinity in two cyanobacteria blooming lakes[J]. Environmental Toxicology and Chemistry, 2018, 37(9): 2312-2322 Walker D, Fathabad S G, Tabatabai B, et al. Microcystin levels in selected cyanobacteria exposed to varying salinity[J]. Journal of Water Resource and Protection, 2019, 11(4): 395-403 李伟, 杨雨玲, 黄松, 等. 产毒与不产毒铜绿微囊藻对模拟酸雨及紫外辐射的生理响应[J]. 生态学报, 2015, 35(23): 7615-7624 Li W, Yang Y L, Huang S, et al. Physiological responses of toxigenic and non-toxigenic strains of Microcystis aeruginosa to simulated acid rain and UV radiation[J]. Acta Ecologica Sinica, 2015, 35(23): 7615-7624(in Chinese)
Zhou J, Qin B Q, Han X X, et al. Turbulence increases the risk of microcystin exposure in a eutrophic lake (Lake Taihu) during cyanobacterial bloom periods[J]. Harmful Algae, 2016, 55: 213-220 Kurmayer R, Christiansen G, Chorus I. The abundance of microcystin-producing genotypes correlates positively with colony size in Microcystis sp. and determines its microcystin net production in Lake Wannsee[J]. Applied and Environmental Microbiology, 2003, 69(2): 787-795 Gan N Q, Xiao Y, Zhu L, et al. The role of microcystins in maintaining colonies of bloom-forming Microcystis spp.[J]. Environmental Microbiology, 2012, 14(3): 730-742 Sedmak B, Elersek T. Microcystins induce morphological and physiological changes in selected representative phytoplanktons[J]. Microbial Ecology, 2006, 51(4): 508-515 Kehr J C, Zilliges Y, Springer A, et al. A mannan binding lectin is involved in cell-cell attachment in a toxic strain of Microcystis aeruginosa[J]. Molecular Microbiology, 2006, 59(3): 893-906 Takaara T, Sasaki S, Fujii M, et al. Lectin-stimulated cellular iron uptake and toxin generation in the freshwater cyanobacterium Microcystis aeruginosa[J]. Harmful Algae, 2019, 83: 25-33 陈何舟, 左胜鹏, 秦伯强, 等. 微囊藻聚集与迁移机制的研究进展[J]. 环境科学与技术, 2019, 42(1): 142-149 Chen H Z, Zuo S P, Qin B Q, et al. Research progress in mechanism of Microcystis aggregation and migration[J]. Environmental Science & Technology, 2019, 42(1): 142-149(in Chinese)
Xiao M, Willis A, Burford M A, et al. Review: A meta-analysis comparing cell-division and cell-adhesion in Microcystis colony formation[J]. Harmful Algae, 2017, 67: 85-91 Phelan R R, Downing T G. The localization of exogenous microcystin LR taken up by a non-microcystin producing cyanobacterium[J]. Toxicon, 2014, 89: 87-90 Makower A K, Schuurmans J M, Groth D, et al. Transcriptomics-aided dissection of the intracellular and extracellular roles of microcystin in Microcystis aeruginosa PCC 7806[J]. Applied and Environmental Microbiology, 2015, 81(2): 544-554 Jüttner F, Lüthi H. Topology and enhanced toxicity of bound microcystins in Microcystis PCC 7806[J]. Toxicon, 2008, 51(3): 388-397 El-Shehawy R, Gorokhova E, Fernández-Piñas F, et al. Global warming and hepatotoxin production by cyanobacteria: What can we learn from experiments?[J]. Water Research, 2012, 46(5): 1420-1429 甘南琴, 魏念, 宋立荣. 微囊藻毒素生物学功能研究进展[J]. 湖泊科学, 2017, 29(1): 1-8 Gan N Q, Wei N, Song L R. Recent progress in research of the biological function of microcystins[J]. Journal of Lake Sciences, 2017, 29(1): 1-8(in Chinese)
Meissner S, Steinhauser D, Dittmann E. Metabolomic analysis indicates a pivotal role of the hepatotoxin microcystin in high light adaptation of Microcystis[J]. Environmental Microbiology, 2015, 17(5): 1497-1509 Yu L, Kong F X, Zhang M, et al. The dynamics of microcystis genotypes and microcystin production and associations with environmental factors during blooms in Lake Chaohu, China[J]. Toxins, 2014, 6(12): 3238-3257 Zhang Y, Jiang H B, Liu S W, et al. Effects of dissolved inorganic carbon on competition of the bloom-forming cyanobacterium Microcystis aeruginosa with the green alga Chlamydomonas microsphaera[J]. European Journal of Phycology, 2012, 47(1): 1-11 Dittmann E, Erhard M, Kaebernick M, et al. Altered expression of two light-dependent genes in a microcystin-lacking mutant of Microcystis aeruginosa PCC 7806[J]. Microbiology, 2001, 147(Pt 11): 3113-3119 Dai R H, Wang P F, Jia P L, et al. A review on factors affecting microcystins production by algae in aquatic environments[J]. World Journal of Microbiology and Biotechnology, 2016, 32(3): 51 Santos A, Rachid C, Pacheco A B, et al. Biotic and abiotic factors affect microcystin-LR concentrations in water/sediment interface[J]. Microbiological Research, 2020, 236: 126452 Schreidah C M, Ratnayake K, Senarath K, et al. Microcystins: Biogenesis, toxicity, analysis, and control[J]. Chemical Research in Toxicology, 2020, 33(9): 2225-2246 Jacinavicius F R, Geraldes V, Crnkovic C M, et al. Effect of ultraviolet radiation on the metabolomic profiles of potentially toxic cyanobacteria[J]. FEMS Microbiology Ecology, 2021, 97(1): fiaa243 Wang B L, Wang X, Hu Y W, et al. The combined effects of UV-C radiation and H2O2 on Microcystis aeruginosa, a bloom-forming cyanobacterium[J]. Chemosphere, 2015, 141: 34-43 Evanthia M, Miquel L, Jutta F, et al. Temperature effects explain continental scale distribution of cyanobacterial toxins[J]. Toxins, 2018, 10(4): 156 Scherer P I, Raeder U, Geist J, et al. Influence of temperature, mixing, and addition of microcystin-LR on microcystin gene expression in Microcystis aeruginosa[J]. MicrobiologyOpen, 2017, 6(1): e00393 Savadova-Ratkus K, Mazur-Marzec H, Karosienė J, et al. Interplay of nutrients, temperature, and competition of native and alien cyanobacteria species growth and cyanotoxin production in temperate lakes[J]. Toxins, 2021, 13(1): 23 Taranu Z E, Pick F R, Creed I F, et al. Meteorological and nutrient conditions influence microcystin congeners in freshwaters[J]. Toxins, 2019, 11(11): 620 Tanvir R U, Hu Z Q, Zhang Y Y, et al. Cyanobacterial community succession and associated cyanotoxin production in hypereutrophic and eutrophic freshwaters[J]. Environmental Pollution, 2021, 290: 118056 Wagner N D, Quach E, Buscho S, et al. Nitrogen form, concentration, and micronutrient availability affect microcystin production in cyanobacterial blooms[J]. Harmful Algae, 2021, 103: 102002 Wang M, Shi W Q, Chen Q W, et al. Effects of nutrient temporal variations on toxic genotype and microcystin concentration in two eutrophic lakes[J]. Ecotoxicology and Environmental Safety, 2018, 166: 192-199 刘雪梅, 章光新. 气候变化对湖泊蓝藻水华的影响研究综述[J]. 水科学进展, 2022, 33(2): 316-326 Liu X M, Zhang G X. A review of studies on the impact of climate change on cyanobacteria blooms in lakes[J]. Advances in Water Science, 2022, 33(2): 316-326(in Chinese)
王成林, 潘维玉, 韩月琪, 等. 全球气候变化对太湖蓝藻水华发展演变的影响[J]. 中国环境科学, 2010, 30(6): 822-828 Wang C L, Pan W Y, Han Y Q, et al. Effect of global climate change on cyanobacteria bloom in Taihu Lake[J]. China Environmental Science, 2010, 30(6): 822-828(in Chinese)
Singo A, Myburgh J G, Laver P N, et al. Vertical transmission of microcystins to Nile crocodile (Crocodylus niloticus) eggs[J]. Toxicon, 2017, 134: 50-56 Gehringer M M, Wannicke N. Climate change and regulation of hepatotoxin production in cyanobacteria[J]. FEMS Microbiology Ecology, 2014, 88(1): 1-25 Dziallas C, Grossart H P. Increasing oxygen radicals and water temperature select for toxic Microcystis sp.[J]. PLoS One, 2011, 6(9): e25569 Bui T, Dao T S, Vo T G, et al. Warming affects growth rates and microcystin production in tropical bloom-forming Microcystis strains[J]. Toxins, 2018, 10(3): 123 Wyner Y, DeSalle R. Distinguishing extinction and natural selection in the anthropocene: Preventing the Panda paradox through practical education measures: We must rethink evolution teaching to prevent misuse of natural selection to biologically justify today's human caused mass extinction crisis[J]. BioEssays: News and Reviews in Molecular, Cellular and Developmental Biology, 2020, 42(2): e1900206 Spalding C, Hull P M. Towards quantifying the mass extinction debt of the Anthropocene[J]. Proceedings Biological Sciences, 2021, 288(1949): 20202332 -

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