Genetic diversity of inorganic carbon uptake systems causes variation in CO2 response of the cyanobacterium Microcystis

ISME Journal

Volumn 8, Issue 3, 2014, Pages 589-600

  Sandrini, Giovanni ^a   Matthijs, Hans C P ^a   Verspagen, Jolanda M H ^a   Muyzer, Gerard ^a   Huisman, Jef ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

bicarbonate transport; climate change; CO2 concentrating mechanism; harmful cyanobacteria; Microcystis aeruginosa; natural selection

Indexed keywords

BICARBONATE; CARBON; CARBON DIOXIDE; SODIUM;

ARTICLE; BACTERIAL GENE; CLASSIFICATION; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROCYSTIS; OPERON; PHYLOGENY;

BICARBONATES; CARBON; CARBON DIOXIDE; GENES, BACTERIAL; GENETIC VARIATION; MICROCYSTIS; OPERON; PHYLOGENY; SODIUM;

EID: 84894365509     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.179     Document Type: Article

References (87)

1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403-410.
2. 2 concentrating mechanism. J Exp Bot 57: 249-265. (Pubitemid 43063780)
3. Balmer MB, Downing JA. (2011). Carbon dioxide concentrations in eutrophic lakes: undersaturation implies atmospheric uptake. Inland Waters 1: 125-132.
4. Bañares-España E, López-Rodas V, Salgado C, Costas E, Flores-Moya A. (2006). Inter-strain variability in the photosynthetic use of inorganic carbon, exemplified by the pH compensation point, in the cyanobacterium Microcystis aeruginosa. Aquat Bot 85: 159-162. (Pubitemid 43850136)
5. Brauer VS, Stomp M, Huisman J. (2012). The nutrient-load hypothesis: patterns of resource limitation and community structure driven by competition for nutrients and light. Am Nat 179: 721-740.
6. Carmichael WW. (2001). Health effects of toxin producing cyanobacteria: the 'CyanoHABS'. Hum Ecol Risk Assess 7: 1393-1407. (Pubitemid 33817358)
7. Chen YW, Qin BQ, Teubner K, Dokulil MT. (2003). Long-term dynamics of phytoplankton assemblages: Microcystis-domination in Lake Taihu, a large shallow lake in China. J Plankton Res 25: 445-453. (Pubitemid 36453369)
8. Chorus I, Bartram J. (1999). Toxic Cyanobacteria in Water: A Guide to their Public Health Consequences, Monitoring and Management. E&FN Spon: London, UK.
9. Codd GA, Morisson LF, Metcalf JS. (2005). Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203: 264-272. (Pubitemid 40311873)
10. Cole JJ, Caraco NF, Kling GW, Kratz TK. (1994). Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568-1570. (Pubitemid 24308969)
11. 2. Plant Cell Environ 29: 1812-1819. (Pubitemid 44141736)
12. Cox PA, Banack SA, Murch SJ. (2003). Biomagnification of cyanobacterial neurotoxins and neurodegenerative disease among the Chamorro people of Guam. Proc Natl Acad Sci USA 100: 13380-13383. (Pubitemid 37444750)
13. Dittmann E, Neilan BA, Erhard M, von Döhren H, Börner T. (1997). Insertional mutagenesis of a peptide synthetase gene that is responsible for hepatotoxin production in the cyanobacterium Microcystis aeruginosa PCC 7806. Mol Microbiol 26: 779-787. (Pubitemid 27489339)
14. Dokulil MT, Teubner K. (2000). Cyanobacterial dominance in lakes. Hydrobiol 438: 1-12. (Pubitemid 32106264)
15. Falconer IR. (2005). Cyanobacterial Toxins in Drinking Water Supplies: Cylindrospermopsins and Micro-cystins. CRC Press: Boca Raton, FL, USA.
16. Frangeul L, Quillardet P, Castets AM, Humbert JF, Matthijs HCP, Cortez D et al. (2008). Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9: 274.
17. 2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Ann Rev Plant Biol 56: 99-131. (Pubitemid 40802405)
18. Gu B, Schelske CL, Coveney MF. (2011). Low carbon dioxide partial pressure in a productive subtropical lake. Aquat Sci 73: 317-330.
19. Gulati RD, van Donk E. (2002). Lakes in the Netherlands, their origin, eutrophication and restoration: state-of-the-art review. Hydrobiologia 478: 73-106. (Pubitemid 35374400)
20. Huisman J, Sharples J, Stroom JM, Visser PM, Kardinaal WEA, Verspagen JMH et al. (2004). Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960-2970. (Pubitemid 39548036)
21. Huisman J, Matthijs HCP, Visser PM (eds) (2005). Harmful Cyanobacteria. Springer: Berlin, Germany.
22. Humbert JH, Barbe V, Latifi A, Gugger M, Calteau A, Coursin T et al. (2013). A tribute to disorder in the genome of the bloom-forming freshwater cyanobacter-ium Microcystis aeruginosa. PLoS One 8: e70747.
23. Ibelings BW, Maberly SC. (1998). Photoinhibition and the availability of inorganic carbon restrict photosynthesis by surface blooms of cyanobacteria. Limnol Oceanogr 43: 408-419. (Pubitemid 28290357)
24. Janse I, Kardinaal WEA, Meima M, Fastner J, Visser PM, Zwart G. (2004). Toxic and nontoxic Microcystis colonies in natural populations can be differentiated on the basis of rRNA gene internal transcribed spacer diversity. Appl Environ Microbiol 70: 3979-3987. (Pubitemid 38969738)
25. Jeppesen E, Søndergaard M, Sortkjær O, Mortensen E, Kristensen P. (1990). Interactions between phytoplank-ton, zooplankton and fish in a shallow, hypertrophic lake: a study of phytoplankton collapses in Lake Søbygård, Denmark. Hydrobiologia 191: 149-164.
26. Jöhnk KD, Huisman J, Sharples J, Sommeijer B, Visser PM, Stroom JM. (2008). Summer heatwaves promote blooms of harmful cyanobacteria. Glob Change Biol 14: 495-512. (Pubitemid 351228524)
27. Kaneko T, Nakajima N, Okamoto S, Suzuki I, Tanabe Y, Tamaoki M et al. (2007). Complete genomic structure of the bloom-forming toxic cyanobacterium Microcystis aeruginosa NIES-843. DNA Res 14: 247-256.
28. 2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539-570. (Pubitemid 129491973)
29. Kardinaal WEA, Tonk L, Janse I, Hol S, Slot P, Huisman J et al. (2007). Competition for light between toxic and nontoxic strains of the harmful cyanobacterium Microcystis. Appl Environ Microb 73: 2939-2946. (Pubitemid 46718577)
30. Kosten S, Huszar VLM, Bécares E, Costa LS, van Donk E, Hansson LA et al. (2012). Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Change Biol 18: 118-126.
31. Lazzarino JK, Bachmann RW, Hoyer MV, Canfield DE. (2009). Carbon dioxide supersaturation in Florida lakes. Hydrobiologia 627: 169-180.
32. Lin S, Haas S, Zemojtel T, Xiao P, Vingron M, Li R. (2011). Genome-wide comparison of cyanobacterial trans-posable elements, potential genetic diversity indicators. Gene 473: 139-149.
33. Long BM, Badger MR, Whitney SM, Price GD. (2007). Analysis of carboxysomes from Synechococcus PCC7942 reveals multiple Rubisco complexes with carboxysomal proteins CcmM and CcaA. J Biol Chem 282: 29323-29335. (Pubitemid 350043344)
34. López-Archilla A, Moreira D, López-García P, Guerrero C. (2004). Phytoplankton diversity and cyanobacterial dominance in a hypereutrophic shallow lake with biologically produced alkaline pH. Extremophiles 8: 109-115. (Pubitemid 40876334)
35. 2 hydration in the cyanobacterium, Synechococcus sp. PCC7942. Mol Microbiol 43: 425-435. (Pubitemid 34146732)
36. Michalak AM, Anderson EJ, Beletsky D, Boland S, Bosche NS, Bridgeman TB et al. (2013). Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci USA 110: 6448-6452.
37. Mitschke J, Georg J, Scholz I, Sharma CM, Dienst D, Bantscheff J et al. (2011). An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc Natl Acad Sci USA 108: 2124-2129.
38. 2-induced activation of the cmp bicarbonate transporter operon by a LysR family protein in the cyanobacterium Synechococcus elongatus strain PCC 7942. Mol Microbiol 68: 98-109. (Pubitemid 351363780)
39. Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T. (1999). Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. strain PCC 7942. Proc Natl Acad Sci USA 96: 13571-13576.
40. Omata T, Takahashi Y, Yamaguchi O, Nishimura T. (2002). Structure, function and regulation of the cyanobacterial high-affinity bicarbonate transporter, BCT1. Funct Plant Biol 29: 151-159. (Pubitemid 34853352)
41. Orr PT, Jones GJ, Douglas GB. (2004). Response of cultured Microcystis aeruginosa from the Swan River, Australia, to elevated salt concentration and consequences for bloom and toxin management in estuaries. Mar Freshw Res 55: 277-283. (Pubitemid 38791353)
42. Otsuka S, Suda S, Shibata S, Oyaizu H, Matsumoto S, Watanabe MM. (2001). A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the Bacteriological Code. Int J Syst Evol Microbiol 51: 873-879. (Pubitemid 32499289)
43. Paerl HW. (2008). Nutrient and other environmental controls of harmful cyanobacterial blooms along the freshwater-marine continuum. Adv Exp Med Biol 619: 217-237.
44. Paerl HW, Huisman J. (2008). Blooms like it hot. Science 320: 57-58.
45. Paerl HW, Ustach J. (1982). Blue-green algal scums: an explanation for their occurrence during freshwater blooms. Limnol Oceanogr 27: 212-217.
46. 2 concentrating mechanism. Photosynth Res 109: 47-57.
47. 2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J Exp Bot 59: 1441-1461. (Pubitemid 351786553)
48. Price GD, Howitt SM. (2011). The cyanobacterial bicarbonate transporter BicA: its physiological role and the implications of structural similarities with human SLC26 transporters. Biochem Cell Biol 89: 178-188.
49. Price GD, Maeda S, Omata T, Badger MR. (2002). Modes of active inorganic carbon uptake in the cyanobacterium, Synechococcus sp. PCC7942. Funct Plant Biol 29: 131-149. (Pubitemid 34853351)
50. Price GD, Shelden MC, Howitt SM. (2011). Membrane topology of the cyanobacterial bicarbonate transporter, SbtA, and identification of potential regulatory loops. Mol Membr Biol 28: 265-275.
51. Price GD, Woodger FJ, Badger MR, Howitt SM, Tucker L. (2004). Identification of a SulP-type bicarbonate transporter in marine cyanobacteria. Proc Natl Acad Sci USA 101: 18228-18233. (Pubitemid 40054102)
52. 2-concentrating mechanism of Synechococcus WH5701 is composed of native and horizontally-acquired components. Photosynth Res 109: 59-72.
53. Raven JA. (2010). Inorganic carbon acquisition by eukar-yotic algae: four current questions. Photosynth Res 106: 123-134.
54. 2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Phil Trans R Soc B 367: 493-507.
55. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. Microbiology 111: 1-61. (Pubitemid 9142236)
56. Robinson NJ, Robinson PJ, Gupta A, Bleasby AJ, Whitton BA, Morby AP. (1995). Singular over-representation of an octameric palindrome, HIP1, in DNA from many cyanobacteria. Nucleic Acids Res 23: 729-735.
57. Robinson PJ, Cranenburgh RM, Head IM, Robinson NJ. (1997). HIP1 propagates in cyanobacterial DNA via nucleotide substitutions but promotes excision at similar frequencies in Escherichia coli and Synechococcus PCC 7942. Mol Microbiol 24: 181-189. (Pubitemid 27160848)
58. Scheffer M. (1998). Ecology of Shallow Lakes. Chapman and Hall: London.
59. 2 promotes phytoplankton productivity. Ecol Lett 7: 446-451. (Pubitemid 38693386)
60. Schwabe W, Weihe A, Börner T, Henning M, Kohl JG. (1988). Plasmids in toxic and nontoxic strains of the cyanobacterium Microcystis aeruginosa. Curr Microbiol 17: 133-137.
61. 2 and pH. Verh Int Ver Theor Angew Limnol 24: 38-54.
62. Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, Fukuzawa H et al. (2002). Genes essential to sodium-dependent bicarbonate transport in cyano-bacteria. J Biol Chem 277: 18658-18664. (Pubitemid 34952421)
63. 2 uptake systems in cyano-bacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc Natl Acad Sci USA 98: 11789-11794. (Pubitemid 32928807)
64. Shively JM, van Keulen G, Meijer WG. (1998). Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu Rev Microbiol 52: 191-230. (Pubitemid 28481192)
65. Smith KS, Ferry JG. (2000). Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24: 335-366.
66. 2 by wild-type cells and ecaA, ecaB, and ccaA mutants of the cyanobacteria Synechococcus PCC7942 and Synechocystis PCC6803. Can J Botany 76: 1153-1160. (Pubitemid 29042849)
67. Sobek S, Tranvik LJ, Cole JJ. (2005). Temperature independence of carbon dioxide supersaturation in global lakes. Global Biogeochem Cycles 19: GB2003.
68. Soltes-Rak E, Mulligan ME, Coleman JR. (1997). Identification and characterization of a gene encoding a vertebrate-type carbonic anhydrase in cyanobacteria. J Bacteriol 179: 769-774. (Pubitemid 27051832)
69. Stumm W, Morgan JJ. (1996). Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters. Wiley-Interscience: New York, NY, USA.
70. Talling JF. (1976). The depletion of carbon dioxide from lake water by phytoplankton. J Ecol 64: 79-121.
71. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
72. Thompson JD, Higgins DG, Gibson TJ. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680. (Pubitemid 24354800)
73. Tonk L, Bosch K, Visser PM, Huisman J. (2007). Salt tolerance of the harmful cyanobacterium Microcystis aeruginosa. Aquat Microb Ecol 46: 117-123. (Pubitemid 46374746)
74. 2. ISME J 5: 1438-1450.
75. Van Gremberghe I, Leliaert F, Mergeay J, Vanormelingen P, Van der Gucht K, Debeer AE et al. (2011). Lack of phylogeographic structure in the freshwater cyano-bacterium Microcystis aeruginosa suggests global dispersal. PLoS One 6: e19561.
76. 2 concentrations affect the elemental stoichiometry and species composition of an experimental phytoplankton community. Freshw Biol 58: 597-611.
77. Verspagen JMH, Passarge J, Jöhnk KD, Visser PM, Peperzak L, Boers P et al. (2006). Water management strategies against toxic Microcystis blooms in the Dutch delta. Ecol Appl 16: 313-327.
78. Visser PM, Passarge J, Mur LR. (1997). Modelling vertical migration of the cyanobacterium Microcystis. Hydrobiologia 349: 99-109.
79. Wallace BB, Bailey MC, Hamilton DP. (2000). Simulation of vertical position of buoyancy regulating Microcystis aeruginosa in a shallow eutrophic lake. Aquat Sci 62: 320-333. (Pubitemid 32122299)
80. Walsby AE, Hayes PK, Boje R, Stal LJ. (1997). The selective advantage of buoyancy provided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. New Phytol 136: 407-417.
81. Wang X, Hao C, Zhang F, Feng C, Yang Y. (2011a). Inhibition of the growth of two-blue-green algae species (Microcystis aruginosa and Anabaena spiroides) by acidification treatments using carbon dioxide. Bioresour Technol 102: 5742-5748.
82. 2 recapture. Photosynth Res 109: 115-122.
83. Wilhelm SW, Boyer GL. (2011). Healthy competition. Nature Clim Change 1: 300-301.
84. 2-concentrating mechanism in a euryhaline, coastal marine cyanobacterium, Synecho-coccus sp. strain PCC 7002: role of NdhR/CcmR. J Bacteriol 189: 3335-3347. (Pubitemid 46668798)
85. Wu X, Wu Z, Song L. (2011). Phenotype and temperature affect the affinity for dissolved inorganic carbon in a cyanobacterium Microcystis. Hydrobiologia 675: 175-186.
86. Xu M, Bernát G, Singh A, Mi H, Rögner M, Pakrasi HB et al. (2008). Properties of mutants of Synechocystis sp. strain PCC 6803 lacking inorganic carbon sequestration systems. Plant Cell Physiol 49: 1672-1677.
87. Zilliges Y, Kehr JC, Meissner S, Ishida K, Mikkat S, Hagemann M et al. (2011). The cyanobacterial hepato-toxin microcystin binds to proteins and increases the fitness of Microcystis under oxidative stress conditions. PloS One 6: e17615.