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Physiological and molecular responses of invasive cyanobacterium Raphidiopsis raciborskii to ambient phosphorus deficiency

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Abstract

Raphidiopsis raciborskii can cause harmful cyanobacterial blooms when concentrations of environmental phosphorus (P) are very low, thus the physiological and molecular mechanisms involved in the acclimation to P need to be characterized better. The growth, chlorophyll fluorescence, alkaline phosphatase, and expression of genes directly involved in P assimilation were compared in the R. raciborskii FACHB 1496 strain grown with and without inorganic P. The specific growth rate (μ), Chl a, and six fluorescence parameters (minimal fluorescence (F0), maximal fluorescence (Fm), maximal variable fluorescence (Fv), electron transport flux (further than QA) per RC (ET0/RC), quantum yield of the electron transport in PSII (ØE0), and the probability that an electron from a trapped exciton is moved into the electron transport chain beyond Q −A (ψ0)) markedly decreased in R. raciborskii in response to experimental P-deficiency. In contrast, the relative variable fluorescence at the J-step (VJ), trapped energy flux (leading to QA reduction) per RC (TR0/RC), and alkaline phosphatase activity significantly increased. In addition, gene expressions involved in the alkaline phosphatase (phoA1 and phoA2), high-affinity inorganic P transporter (pstS1), phosphonate transporter and metabolism (phnD and phnM), and nucleotidase (nucH) were significantly upregulated under P deficiency. However, physiological and molecular responses were resumed rapidly after P re-supplementation following P-deficient conditions. Our results highlight that R. raciborskii can perform coordinated and complex cellular and physiological responses to cope with P deficiency, reflecting R. raciborskii’s multi-faceted machinery to respond to environmental P fluctuations.

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Data Availability Statement

The authors declare that all data supporting the findings of this study are available within the article. The raw data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Alexander H, Rouco M, Haley S T et al. 2015. Functional group-specific traits drive phytoplankton dynamics in the oligotrophic ocean. Proceedings of the National Academy of Sciences of the United States of America, 112(44): E5972–E5979.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Bai F, Liu R, Yang Y J et al. 2014. Dissolved organic phosphorus use by the invasive freshwater diazotroph cyanobacterium, Cylindrospermopsis raciborskii. Harmful Algae, 39: 112–120.

    Article  Google Scholar 

  • Bai F, Shi J Q, Yang S Q et al. 2020. Interspecific competition between Cylindrospermopsis raciborskii and Microcystis aeruginosa on different phosphorus substrates. Environmental Science and Pollution Research, 27(34): 42264–42275.

    Article  Google Scholar 

  • Beszteri S, Yang I, Jaeckisch N et al. 2012. Transcriptomic response of the toxic prymnesiophyte Prymnesium parvum (N. Carter) to phosphorus and nitrogen starvation. Harmful Algae, 18: 1–15.

    Article  Google Scholar 

  • Burford M A, Beardall J, Willis A et al. 2016. Understanding the winning strategies used by the bloom-forming cyanobacterium Cylindrospermopsis raciborskii. Harmful Algae, 54: 44–53.

    Article  Google Scholar 

  • Burford M A, Davis T W, Orr P T et al. 2014. Nutrient-related changes in the toxicity of field blooms of the cyanobacterium, Cylindrospermopsis raciborskii. FEMS Microbiology Ecology, 89(1): 135–148.

    Article  Google Scholar 

  • Burford M A, Willis A, Chuang A et al. 2018. Recent insights into physiological responses to nutrients by the cylindrospermopsin producing cyanobacterium, Cylindrospermopsis raciborskii. Journal of Oceanology and Limnology, 36(4): 1032–1039.

    Article  Google Scholar 

  • Carpenter S R, Caraco N F, Correll D L et al. 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications, 8(3): 559–568.

    Article  Google Scholar 

  • Chislock M F, Sharp K L, Wilson A E. 2014. Cylindrospermopsis raciborskii dominates under very low and high nitrogen-to-phosphorus ratios. Water Research, 49: 207–214.

    Google Scholar 

  • Downing J A, McCauley E. 1992. The nitrogen: phosphorus relationship in lakes. Limnology and Oceanography, 37(5): 936–945.

    Article  Google Scholar 

  • Droop M R. 1973. Some thoughts on nutrient limitation in algae. Journal of Phycology, 9(3): 264–272.

    Article  Google Scholar 

  • Dyhrman S T, Chappell P D, Haley S T et al. 2006. Phosphonate utilization by the globally important marine diazotroph Trichodesmium. Nature, 439(7072): 68–71.

    Article  Google Scholar 

  • Dyhrman S T, Jenkins B D, Rynearson T A et al. 2012. The transcriptome and proteome of the diatom Thalassiosira pseudonana reveal a diverse phosphorus stress response. PLoS One, 7(3): e33768.

    Article  Google Scholar 

  • Dyhrman S T, Palenik B. 2003. Characterization of ectoenzyme activity and phosphate-regulated proteins in the coccolithophorid Emiliania huxleyi. Journal of Plankton Research, 25(10): 1215–1225.

    Article  Google Scholar 

  • Dyhrman S T. 2016. Nutrients and their acquisition: phosphorus physiology in microalgae. In: Borowitzka M A, Beardall J, Raven J A eds. The Physiology of Microalgae. Springer, Cham. p.155–183.

    Chapter  Google Scholar 

  • Elser J J, Elser M M, MacKay N A et al. 1988. Zooplanktonmediated transitions between N- and P-limited algal growth. Limnology and Oceanography, 33(1): 1–14.

    Article  Google Scholar 

  • Frischkorn K R, Harke M J, Gobler C J et al. 2014. De novo assembly of Aureococcus anophagefferens transcriptomes reveals diverse responses to the low nutrient and low light conditions present during blooms. Frontiers in Microbiology, 5: 375.

    Google Scholar 

  • Fuentes-Valdés J J, Plominsky A M, Allen E E et al. 2016. Complete genome sequence of a Cylindrospermopsin-Producing cyanobacterium, Cylindrospermopsis raciborskii CS505, containing a circular chromosome and a single extrachromosomal element. Genome Announcements, 4(4): e00823–16.

    Article  Google Scholar 

  • González-Gil S, Keafer B A, Jovine R V M et al. 1998. Detection and quantification of alkaline phosphatase in single cells of phosphorus-starved marine phytoplankton. Marine Ecology Progress Series, 164: 21–35.

    Article  Google Scholar 

  • Guedes I A, Pacheco A B F, Vilar M C P et al. 2019. Intraspecific variability in response to phosphorus depleted conditions in the cyanobacteria Microcystis aeruginosa and Raphidiopsis raciborskii. Harmful Algae, 86: 96–105.

    Article  Google Scholar 

  • Hamilton D P, Salmaso N, Paerl H W. 2016. Mtigating harmful cyanobacterial blooms: strategies for control of nitrogen and phosphorus loads. Aquatic Ecology, 50(3): 351–366.

    Article  Google Scholar 

  • Harke M J, Berry D L, Ammerman J W et al. 2012. Molecular response of the bloom-forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microbial Ecology, 63(1): 188–198.

    Article  Google Scholar 

  • Harke M J, Gobler C J. 2013. Global transcriptional responses of the toxic cyanobacterium, Microcystis aeruginosa, to nitrogen stress, phosphorus stress, and growth on organic matter. PLoS One, 8(7): e69834.

    Article  Google Scholar 

  • Ichimura T. 1979. Isolation and culture methods of algae. In: Nishizawa K, Chihara M eds. Methods in Phycological Studies. Kyoritsu Shuppan, Tokyo. p.294–305. (in Japanese)

    Google Scholar 

  • Ilikchyan I N, McKay R M L, Zehr J P et al. 2009. Detection and expression of the phosphonate transporter gene phnD in marine and freshwater picocyanobacteria. Environmental Microbiology, 11(5): 1314–1324.

    Article  Google Scholar 

  • Isvánovics V, Shafik H M, Présing M et al. 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (Cyanophyceae) in throughflow cultures. Freshwater Biology, 43(2): 257–275.

    Article  Google Scholar 

  • Jacob J, Lawlor D W. 1993. In vivo photosynthetic electron transport does not limit photosynthetic capacity in phosphate-deficient sunflower and maize leaves. Plant, Cell & Environment, 16(7): 785–795.

    Article  Google Scholar 

  • Jacob J. 1995. Phosphate deficiency increases the rate constant of thermal dissipation of excitation energy by Photosystem II in intact leaves of sunflower and maize. Australian Journal of Plant Physiology, 22(3): 417–424.

    Google Scholar 

  • Karl D M. 2014. Microbially mediated transformations of phosphorus in the sea: new views of an old cycle. Annual Review of Marine Science, 6: 279–337.

    Article  Google Scholar 

  • Li M Z, Shi X G, Guo C T et al. 2016. Phosphorus deficiency inhibits cell division but not growth in the dinoflagellate Amphidinium carterae. Frontiers in Microbiology, 7: 826.

    Google Scholar 

  • Lin S J, Litaker R W, Sunda W G. 2016. Phosphorus physiological ecology and molecular mechanisms in marine phytoplankton. Journal of Phycology, 52(1): 10–36.

    Article  Google Scholar 

  • Lin X, Zhang H, Huang B Q et al. 2012. Alkaline phosphatase gene sequence characteristics and transcriptional regulation by phosphate limitation in Karenia brevis (Dinophyceae). Harmful Algae, 17: 14–24.

    Article  Google Scholar 

  • Liu Z F, Koid A E, Terrado R et al. 2015. Changes in gene expression of Prymnesium parvum induced by nitrogen and phosphorus limitation. Frontiers in Microbiology, 6: 631.

    Article  Google Scholar 

  • Liu Z Y, Wu C D. 2012. Response of alkaline phosphatases in the cyanobacterium Anabaena sp. FACHB 709 to inorganic phosphate starvation. Current Microbiology, 64(6): 524–529.

    Article  Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the method. Methods, 25(4): 402–408.

    Article  Google Scholar 

  • Lu Z, Lei L M, Lu Y et al. 2021. Phosphorus deficiency stimulates dominance of Cylindrospermopsis through facilitating cylindrospermopsin-induced alkaline phosphatase secretion: integrating field and laboratory-based evidences. Environmental Pollution, 290: 117946.

    Article  Google Scholar 

  • Luo H, Lin X, Li L et al. 2017. Transcriptomic and physiological analyses of the dinoflagellate Karenia mikimotoi reveal non-alkaline phosphatase-based molecular machinery of ATP utilisation. Environmental Microbiology, 19(11): 4506–4518.

    Article  Google Scholar 

  • Moore L R, Ostrowski M, Scanlan D J et al. 2005. Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria. Aquatic Microbial Ecology, 39(3): 257–269.

    Article  Google Scholar 

  • Nausch M, Nausch G, Wasmund N. 2004. Phosphorus dynamics during the transition from nitrogen to phosphate limitation in the central Baltic Sea. Marine Ecology Progress Series, 266: 15–25.

    Article  Google Scholar 

  • Nusch E A. 1980. Comparison of different methods for chlorophyll and phaeopigment determination. Archiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie, 14: 14–36.

    Google Scholar 

  • Padisák J. 1997. Cylindrospermopsis raciborskii (Woloszaynska) Seenaya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv für Hydrobiologie, 107(S1): 563–593.

    Google Scholar 

  • Paerl H W, Xu H, McCarthy M J et al. 2011. Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Research, 45(5): 1973–1983.

    Article  Google Scholar 

  • Perron M C, Qiu B S, Boucher N et al. 2012. Use of chlorophyll a fluorescence to detect the effect of microcystins on photosynthesis and photosystem II energy fluxes of green algae. Toxicon, 59(5): 567–577.

    Article  Google Scholar 

  • Piccini C, Aubriot L, Fabre A et al. 2011. Genetic and eco-physiological differences of South American Cylindrospermopsis raciborskii isolates support the hypothesis of multiple ecotypes. Harmful Algae, 10(6): 644–653.

    Article  Google Scholar 

  • Pierangelini M, Stojkovic S, Orr P T et al. 2014. Photosynthetic characteristics of two Cylindrospermopsis raciborskii strains differing in their toxicity. Journal of Phycology, 50(2): 292–302.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Prentice M J, Hamilton D P, Willis A et al. 2019. Quantifying the role of organic phosphorus mineralisation on phytoplankton communities in a warm-monomictic lake. Inland Waters, 9(1): 10–24.

    Article  Google Scholar 

  • Prentice M J, O’Brien K R, Hamilton D P et al. 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.

    Article  Google Scholar 

  • Qin B Q, Xu P Z, Wu Q L et al. 2007. Environmental issues of Lake Taihu, China. Hydrobiologia, 581(1): 3–14.

    Article  Google Scholar 

  • Saker M L, Griffiths D J. 2001. Occurrence of blooms of the cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenayya and Subba Raju in a north Queensland domestic water supply. Marine and Freshwater Research, 52(6): 907–915.

    Article  Google Scholar 

  • Sebastian M, Ammerman J W. 2009. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. The ISME Journal, 3(5): 563–572.

    Article  Google Scholar 

  • Shen H, Song L R. 2007. Comparative studies on physiological responses to phosphorus in two phenotypes of bloom-forming Microcystis. Hydrobiologia, 592(1): 475–486.

    Article  Google Scholar 

  • Shi X G, Lin X, Li L et al. 2017. Transcriptomic and microRNAomic profiling reveals multi-faceted mechanisms to cope with phosphate stress in a dinoflagellate. The ISME Journal, 11(10): 2209–2218.

    Article  Google Scholar 

  • Sinha R, Pearson L A, Davis T W et al. 2014. Comparative genomics of Cylindrospermopsis raciborskii strains with differential toxicities. BMC Genomics, 15: 83.

    Article  Google Scholar 

  • Smith V H. 1983. Low nitrogen to phosphorus ratios favor dominance by blue-green algae in lake phytoplankton. Science, 221(4611): 669–671.

    Article  Google Scholar 

  • Strasser B J, Strasser R J. 1995. Measuring fast fluorescence transients to address environmental questions: the JIP test. In: Mathis P ed. Photosynthesis: from Light to Biosphere. KAP Press, Dordrecht. p.977–980.

    Google Scholar 

  • Stucken K, John U, Cembella A et al. 2010. The smallest known genomes of multicellular and toxic cyanobacteria: comparison, minimal gene sets for linked traits and the evolutionary implications. PLoS One, 5(2): e9235.

    Article  Google Scholar 

  • Su Z C, Dam P, Chen X et al. 2003. Computational inference of regulatory pathways in microbes: an application to phosphorus assimilation pathways in Synechococcus sp. WH8102. Genome Informatics, 13: 3–13.

    Google Scholar 

  • Su Z S, Olman V, Xu Y. 2007. Computational prediction of Pho regulons in cyanobacteria. BMC Genomics, 8: 156.

    Article  Google Scholar 

  • Suzuki S, Ferjani A, Suzuki L et al. 2004. The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in Synechocystis. Journal of Biological Chemistry, 279(13): 13234–13240.

    Article  Google Scholar 

  • Tetu S G, Brahamsha B, Johnson D A et al. 2009. Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. The ISME Journal, 3(7): 835–849.

    Article  Google Scholar 

  • Vershinina O A, Znamenskaya L V. 2002. The Pho regulons of bacteria. Microbiology, 71(5): 497–511.

    Article  Google Scholar 

  • Wan L L, Chen X Y, Deng Q H et al. 2019. Phosphorus strategy in bloom-forming cyanobacteria (Dolichospermum and Microcystis) and its role in their succession. Harmful Algae, 84: 46–55.

    Article  Google Scholar 

  • Welch E B, Cooke G D. 1995. Internal phosphorus loading in shallow lakes: importance and control. Lake and Reservoir Management, 11(3): 273–281.

    Article  Google Scholar 

  • Willis A, Adams M P, Chuang A W et al. 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.

    Article  Google Scholar 

  • Willis A, Chuang A W, Dyhrman S et al. 2019. Differential expression of phosphorus acquisition genes in response to phosphorus stress in two Raphidiopsis raciborskii strains. Harmful Algae, 82: 19–25.

    Article  Google Scholar 

  • Willis A, Posselt A J, Burford M A. 2017. Variations in carbon-to-phosphorus ratios of two Australian strains of Cylindrospermopsis raciborskii. European Journal of Phycology, 52(3): 303–310.

    Article  Google Scholar 

  • Willis A, Woodhouse J N, Ongley S E et al. 2018. Genome variation in nine co-occurring toxic Cylindrospermopsis raciborskii strains. Harmful Algae, 73: 157–166.

    Article  Google Scholar 

  • Wu J F, Sunda W, Boyle E A et al. 2000. Phosphate depletion in the western North Atlantic Ocean. Science, 289(5480): 759–762.

    Article  Google Scholar 

  • Wu J R, Shien J H, Shieh H K et al. 2007. Cloning of the gene and characterization of the enzymatic properties of the monomeric alkaline phosphatase (phoX) from Pasteurella multocida strain X-73. FEMS Microbiology Letters, 267(1): 113–120.

    Article  Google Scholar 

  • Wu Z X, Shi J Q, Li R H. 2009. Comparative studies on photosynthesis and phosphate metabolism of Cylindrospermopsis raciborskii with Microcystis aeruginosa and Aphanizomenon flos-aquae. Harmful Algae, 8(6): 910–915.

    Article  Google Scholar 

  • Wu Z X, Shi J Q, Lin S et al. 2010. Unraveling molecular diversity and phylogeny of Aphanizomenon (Nostocales, Cyanobacteria) strains isolated from China. Journal of Phycology, 46(5): 1048–1058.

    Article  Google Scholar 

  • Wu Z X, Zeng B, Li R H et al. 2012. Physiological regulation of Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria) in response to inorganic phosphorus limitation. Harmful Algae, 15: 53–58.

    Article  Google Scholar 

  • Xiao M, Hamilton D P, Chuang A et al. 2020. Intra-population strain variation in phosphorus storage strategies of the freshwater cyanobacterium Raphidiopsis raciborskii. FEMS Microbiology Ecology, 96(6): fiaa092.

    Article  Google Scholar 

  • Xu H, Paerl H W, Qin B Q et al. 2010. Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography, 55(1): 420–432.

    Article  Google Scholar 

  • Yang Y J, Shi J Q, Jia Y L et al. 2020. Unveiling the impact of glycerol phosphate (DOP) in the dinoflagellate Peridinium bipes by physiological and transcriptomic analysis. Environmental Sciences Europe, 32(1): 38.

    Article  Google Scholar 

  • Young E B, Tucker R C, Pansch L A. 2010. Alkaline phosphatase in freshwater Cladophora-epiphyte assemblages: regulation in response to phosphorus supply and localization. Journal of Phycology, 46(1): 93–101.

    Article  Google Scholar 

  • Zhang C Y, Chen G F, Wang Y Y et al. 2018. Physiological and molecular responses of Prorocentrum donghaiense to dissolved inorganic phosphorus limitation. Marine Pollution Bulletin, 129(2): 562–572.

    Article  Google Scholar 

  • Zhang S F, Yuan C J, Chen Y et al. 2016. Comparative transcriptomic analysis reveals novel insights into the adaptive response of Skeletonema costatum to changing ambient phosphorus. Frontiers in Microbiology, 7: 1476.

    Article  Google Scholar 

  • Zhang S F, Yuan C J, Chen Y et al. 2019. Transcriptomic response to changing ambient phosphorus in the marine dinoflagellate Prorocentrum donghaiense. Science of the Total Environment, 692: 1037–1047.

    Article  Google Scholar 

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  1. Key Laboratory of Eco-environments in Three Gorges Reservoir Region (Ministry of Education), Chongqing Key Laboratory of Plant Ecology and Resources Research in Three Gorges Reservoir Region, School of Life Sciences, Southwest University, Chongqing, 400715, China

    Junqiong Shi, Shuhan He, Lu Zhao, Lulu Ji, Songqi Yang & Zhongxing Wu

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Supported by the National Natural Science Foundation of China (Nos. 42177055, 41877410) and the Chongqing Postgraduate Scientific Research Innovation Project (Nos. CYS21106, CYS20105)

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Shi, J., He, S., Zhao, L. et al. Physiological and molecular responses of invasive cyanobacterium Raphidiopsis raciborskii to ambient phosphorus deficiency. J. Ocean. Limnol. 40, 1792–1803 (2022). https://doi.org/10.1007/s00343-022-1314-z

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