A bacterial pathogen displaying temperature-enhanced virulence of the microalga Emiliania huxleyi

Frontiers in Microbiology

Volumn 7, Issue JUN, 2016, Pages

  Mayers, Teaghan J ^a   Bramucci, Anna R ^a   Yakimovich, Kurt M ^a   Case, Rebecca J ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Climate change; Emiliania huxleyi; Marine pathogen; Ocean warming; Phytoplankton; Roseobacter; Ruegeria; Temperature enhanced virulence

Indexed keywords

AMPLITUDE MODULATION; APOPTOSIS; ARTICLE; AUTOFLUORESCENCE IMAGING; BACTERIAL VIRULENCE; BACTERIUM CONTAMINATION; CELL DENSITY; CHLOROPHYLL CONTENT; CLIMATE CHANGE; COLONY FORMING UNIT; CONTROLLED STUDY; EMILIANIA HUXLEYI; FLUORESCENCE; FLUORESCENCE ACTIVATED CELL SORTING; MICROALGA; NONHUMAN; POPULATION DENSITY; TEMPERATURE;

EID: 84980051732     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00892     Document Type: Article

References (64)

1. Ashen, J. B., and Goff, L. J. (1998). Galls on the marine red alga Prionitis laceolata (Halymeniaceae): specific induction and subsequent development of an algal-bacterial symbiosis. Am. J. Bot. 85, 1710-1721. doi: 10.2307/2446505
2. Ashen, J. B., and Goff, L. J. (2000). Molecular and ecological evidence for species specificity and coevolution in a group of marine algal-bacterial symbioses. Appl. Environ. Microbiol. 66, 3024-3030. doi: 10.1128/AEM.66.7.3024-3030.2000
3. Ayers, G. P., and Cainey, J. M. (2007). The CLAW hypothesis: a review of the major developments. Environ. Chem. 4, 366-374. doi: 10.1071/EN07080
4. Behrenfeld, M. J., Randerson, J. T., McClain, C. R., Feldman, G. C., Los, S. O., Tucker, C. J., et al. (2001). Biospheric primary production during an ENSO transition. Science 291, 2594-2597. doi: 10.1126/science.1055071
5. Ben-Haim, Y., Zicherman-Keren, M., and Rosenberg, E. (2003). Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl. Environ. Microbiol. 69, 4236-4242. doi: 10.1128/AEM.69.7.4236-4242.2003
6. Bidle, K. D., Haramaty, L., Barcelos, E., Ramos, J., and Falkowski, P. (2007). Viral activation and recruitment of metacaspases in the unicellular coccolithophore, Emiliania huxleyi. Proc. Natl. Acad. Sci. U.S.A. 104, 6049-6054. doi: 10.1073/pnas.0701240104
7. Bidle, K. D., and Kwityn, C. J. (2012). Assessing the role of caspase activity and metacaspase expression on viral susceptibility of the coccolithophore, Emiliania huxleyi (Haptophyta). J. Phycol. 48, 1079-1089. doi: 10.1111/j.1529-8817.2012.01209.x
8. Boyce, D. G., Lewis, M. R., and Worm, B. (2010). Global phytoplankton decline over the past century. Nature 466, 591-596. doi: 10.1038/nature09268
9. Bramucci, A. R., Labeeuw, L., Mayers, T. J., Saby, J. A., and Case, R. J. (2015). A small volume bioassay to assess bacterial/phytoplankton co-culture using WATER-Pulse-Amplitude-Modulated (WATER-PAM) fluorometry. J. Vis. Exp. 97:e52455. doi: 10.3791/52455
10. Brown, C. W., and Yoder, J. A. (1994). Coccolithophorid blooms in the global ocean. J. Geophys. Res. 99, 7467-7482. doi: 10.1029/93JC02156
11. Budde, I. P., and Ullrich, M. S. (2000). Interactions of Pseudomonas syringae pv. glycinea with host and nonhost plants in relation to temperature and phytotoxin synthesis. Mol. Plant Microbe Interact 13, 951-961. doi: 10.1094/MPMI.2000.13.9.951
12. Case, R. J., Longford, S. R., Campbell, A. H., Low, A., Tujula, N., Steinberg, P. D., et al. (2011). Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga. Environ. Microbiol. 13, 529-537. doi: 10.1111/j.1462-2920.2010.02356.x
13. Charlson, R. J., Lovelock, J. E., Andreae, M. O., and Warren, S. G. (1987). Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate. Nature 326, 655-661. doi: 10.1038/326655a0
14. Choi, C. J., and Berges, J. A. (2013). New types of metacaspases in phytoplankton reveal diverse origins of cell death proteases. Cell Death Dis. 4, 1-7. doi: 10.1038/cddis.2013.21
15. Chow, J. S., Lee, C., and Engel, A. (2015). The influence of extracellular polysaccharides, growth rate, and free coccoliths on the coagulation efficiency of Emiliania huxleyi. Mar. Chem. 175, 5-17. doi: 10.1016/j.marchem.2015.04.010
16. Coll, N. S., Epple, P., and Dangl, J. L. (2011). Programmed cell death in the plant immune system. Cell Death Differ. 18, 1247-1256. doi: 10.1038/cdd.2011.37
17. Daniels, C. J., Sheward, R. M., and Poulton, A. J. (2014). Biogeochemical implications of comparative growth rates of Emiliania huxleyi and Coccolithus species. Biogeosciences 11, 6915-6925. doi: 10.5194/bg-11-6915-2014
18. Douglas, A. E. (2003). Coral bleaching-how and why? Ma. Pollut. Bull. 46, 385-392. doi: 10.1016/S0025-326X(03)00037-7
19. Egan, S., Harder, T., Burke, C., Steinberg, P., Kjelleberg, S., and Thomas, T. (2013). The seaweed holobiont: understanding seaweed-bacteria interactions. FEMS Microbiol. Rev. 37, 462-476. doi: 10.1111/1574-6976.12011
20. Fernandes, N., Case, R. J., Longford, S. R., Seyedsayamdost, M. R., Steinberg, P. D., Kjelleberg, S., et al. (2011). Genomes and virulence factors of novel bacterial pathogens causing bleaching disease in the marine red alga Delisea pulchra. PLoS ONE 6:e27387. doi: 10.1371/journal.pone.0027387
21. Frada, M., Probert, I., Allen, M. J., Wilson, W. H., and de Vargas, C. (2008). The "Cheshire Cat" escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proc. Natl. Acad. Sci. U.S.A. 105, 15944-15949. doi: 10.1073/pnas.0807707105
22. Frada, M. J., Bidle, K. D., Probert, I., and de Vargas, C. (2012). In situ survey of life cycle phases of the coccolithophore Emiliania huxleyi (Haptophyta). Environ. Microbiol. 14, 1558-1569. doi: 10.1111/j.1462-2920.2012.02745.x
23. Fulton, J. M., Fredricks, H. F., Bidle, K. D., Vardi, A., Kendrick, B. J., DiTullio, G. R., et al. (2014). Novel molecular determinants of viral susceptibility and resistance in the lipidome of Emiliania huxleyi. Environ. Microbiol. 16, 1137-1149. doi: 10.1111/1462-2920.12358
24. Gao, K., Ruan, Z., Villafane, V. E., Gattuso, J., and Helbling, E. W. (2009). Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 54, 1855-1862. doi: 10.4319/lo.2009.54.6.1855
25. Gardiner, M., Thomas, T., and Egan, S. (2015). A glutathione peroxidase (GpoA) plays a role in the pathogenicity of Nautella italica strain R11 towards the red alga Delisea pulchra. FEMS Microbiol. Ecol. 91:fiv021. doi: 10.1093/femsec/fiv021
26. Gonzalez, J. M., Simo, R., Massana, R., Covert, J. S., Casamayor, E. O., Pedros-Alio, C., et al. (2000). Bacterial community structure associated with a dimethylsulfoniopropionate-producing North Atlantic algal bloom. Appl. Environ. Microbiol. 66, 4237-4246. doi: 10.1128/AEM.66.10.4237-4246.2000
27. Green, D. H., Echavarri-Bravo, V., Brennan, D., and Hart, M. C. (2015). Bacterial diversity associated with the coccolithophorid algae Emiliania huxleyi and Coccolithus pelagicus f. braarudii. Biomed. Res. Int. 2015, 1-15. doi: 10.1155/2015/194540
28. Green, J. C., Course, P. A., and Tarran, G. A. (1996). The life-cycle of Emiliania huxleyi: a brief review and a study of ploidy levels analysed by flow cytometry. J. Mar. Syst. 9, 33-44. doi: 10.1016/0924-7963(96)00014-0
29. Guillard, R. R. L., and Hargraves, P. E. (1993). Stichochrysis immobilis is a diatom, not a chrysophyte. Phycologia 32, 234-236. doi: 10.2216/i0031-8884-32-3-234.1
30. Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., et al. (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158-2162. doi: 10.1126/science.1063699
31. Helliwell, K. E., Wheeler, G. L., Leptos, K. C., Goldstein, R. E., and Smith, A. G. (2011). Insights into the evolution of vitamin B12 auxotrophy from sequenced algal genomes. Mol. Biol. Evol. 28, 1-13. doi: 10.1093/molbev/msr124
32. Huisman, J. (2000). Marine Plants of Australia. Nedlands, WA: University of Western Australia Press.
33. Jenkins, S. R., Hawkins, S. J., and Norton, T. A. (1999). Direct and indirect effects of a macroalgal canopy and limpet grazing in structuring a sheltered inter-tidal community. Mar. Ecol. Prog. Ser. 188, 81-92. doi: 10.3354/meps188081
34. Kendrick, B. J., DiTullio, G. R., Cyronak, T. J., Fulton, J. M., Van Mooy, B. A., and Bidle, K. D. (2014). Temperature-induced viral resistance in Emiliania huxleyi (Prymnesiophyceae). PLoS ONE 9:e112134. doi: 10.1371/journal.pone.0112134
35. Kushmaro, A., Loya, Y., Fine, M., and Rosenberg, E. (1996). Bacterial infection and coral bleaching. Nature 380:396. doi: 10.1038/380396a0
36. Labeeuw, L., Khey, J., Bramucci, A. R., Atwal, H., de la Mata, P., Haryunk, J., et al. (2016). Indole-3-acetic acid is produced by Emiliania huxleyi cocolith-bearing cells and triggers a physiological response in bald cells. Front. Microbiol. 7:828. doi: 10.3389/fmicb.2016.00828
37. Lam, E., Kato, N., and Lawton, M. (2001). Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848-853. doi: 10.1038/35081184
38. Madeo, F., Herker, E., Maldener, C., Klissing, S., Lachelt, S., Herlan, M., et al. (2002). A caspase-related protease regulated apoptosis in yeast. Mol. Cell. 9, 911-917.
39. Oliver, E. C. J., Wotherspoon, S. J., Chamberlain, M. A., and Holbrook, N. J. (2014). Projected Tasman Sea extremes in sea surface temperature through the twenty-first century. J. Climate 27, 1980-1998. doi: 10.1175/JCLI-D-13-00259.1
40. Paasche, E. (2002). A review of the coccolithophorid Emiliania huxleyi (Prymnesiophyceae), with particular reference to growth, coccolith formation, and calcification-photosynthesis interactions. Phycologia 40, 503-529. doi: 10.2216/i0031-8884-40-6-503.1
41. Quinn, P. K., and Bates, T. S. (2011). The case against climate regulation via oceanic phytoplankton sulphur emissions. Nature 480, 51-56. doi: 10.1038/nature10580
42. Reisch, C. R., Moran, M. A., and Whitman, W. B. (2011). Bacterial catabolism of dimethylsulfoniopropionate (DMSP). Front. Microbiol. 2:172. doi: 10.3389/fmicb.2011.00172
43. Rhodes, L. L., Peake, B. M., MacKenzie, A. L., and Marwick, S. (1995). Coccolithophores Gephyrocapsa oceanica and Emiliania huxleyi (Prymnesiophyceae=Haptophyceae) in New Zealand's coastal waters: characteristics of blooms and growth in laboratory culture. N. Z. J. Mar. Freshw. Res. 29, 345-357. doi: 10.1080/00288330.1995.9516669
44. Rosenberg, E., Kushmaro, A., Kramarsky-Winter, E., Banin, E., and Yossi, L. (2009). The role of microorganisms in coral bleaching. ISME J. 3, 139-146. doi: 10.1038/ismej.2008.104
45. Sapp, M., Schwaderer, A. S., Wiltshire, K. H., Hoppe, H. G., Gerdts, G., and Wichels, A. (2007). Species-specific bacterial communities in the phycosphere of microalgae? Microb Ecol. 53, 1-17. doi: 10.1007/s00248-006-9162-5
46. Schmidt, S., Harlay, J., Borges, A. V., Groome, S., Delilled, B., Roevros, N., et al. (2013). Particle export during a bloom of Emiliania huxleyi in the North-West European continental margin. J. Mar. Syst. 109-110, 182-190. doi: 10.1016/j.jmarsys.2011.12.005
47. Schreiber, U. (1998). Chlorophyll fluorescence: new instruments for special applications. Photosynthesis Mech. Effects 5, 4253-4258.
48. Schreiber, U., Schliwa, U., and Bilger, W. (1986). Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Res. 10, 51-62. doi: 10.1007/BF00024185
49. Seyedsayamdost, M. R., Case, R. J., Kolter, R., and Clardy, J. (2011). The Jekyll-and-Hyde chemistry of Phaeobacter gallaeciensis. Nat. Chem. 3, 331-335. doi: 10.1038/nchem.1002
50. Simó, R. (2004). From cells to globe: approaching the dynamics of DMS(P) in the ocean at multiple scales. Can. J. Fisheries Aquat. Sci. 61, 673-684. doi: 10.1139/f04-030
51. Smirnova, A., Li, H., Weingart, H., Aufhammer, S., Burse, A., Finis, K., et al. (2001). Thermoregulated expression of virulence factors in plant-associated bacteria. Arch. Microbiol. 176, 393-399. doi: 10.1007/s002030100344
52. Smith, T. M., Reynolds, R. W., Peterson, T. C., and Lawrimore, J. (2008). Improvements to NOAA's Historical Merged Land-Ocean Surface Temperature Analysis (1880-2006). J. Climate 21, 2283-2296. doi: 10.1175/2007JCLI2100.1
53. Sundström, J. F., Vaculova, A., Smertenko, A. P., Savenkov, E. I., Golovko, A., Minina, E., et al. (2009). Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat. Cell Biol. 11, 1347-1354. doi: 10.1038/ncb1979
54. Thrall, P. H., Burdon, J. J., and Young, A. (2001). Variation in resistance and virulence among demes of a plant host-pathogen metapopulation. J. Ecol. 86, 736-748. doi: 10.1111/j.1461-0248.2012.01749.x
55. van Kooten, O., and Snel, J. F. H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Res. 25, 147-150. doi: 10.1007/BF00033156
56. Vardi, A., Van Mooy, B. A., Fredricks, H. F., Popendorf, K. J., Ossolinski, J. E., Haramaty, L., et al. (2009). Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326, 861-865. doi: 10.1126/science.1177322
57. von Dassow P., John, U., Ogata, H., Probert, I., Bendif, M., Kegel, J. U., et al. (2015). Life-cycle modification in open oceans accounts for genome variability in a cosmopolitan phytoplankton. ISME J. 9, 1365-1377. doi: 10.1038/ismej.2014.221
58. von Dassow P., Ogata, H., Probert, I., Wincker, P., Da, Silva, C., Audic, S., et al. (2009). Transcriptome analysis of functional differentiation between haploid and diploid cells of Emiliania huxleyi, a globally significant photosynthetic calcifying cell. Genome Biol. 10, 1-33. doi: 10.1186/gb-2009-10-10-r114
59. Voss, K. J., Balch, W. M., and Kilpatrick, K. A. (1998). Scattering and attenuation properties of Emiliania huxleyi cells and their detached coccoliths. Limnol. Oceanogr. 43, 870-876. doi: 10.4319/lo.1998.43.5.0870
60. Webb, A. L., Malin, G., Hopkins, F. E., Ho, K. L., Riebesell, U., Schulz, K. G., et al. (2016). Ocean acidification has different effects on the production of dimethylsulfide and dimethylsulfoniopropionate measured in cultures of Emiliania huxleyi and a mesocosm study: a comparison of laboratory monocultures and community interactions. Environ. Chem. 13, 314-329. doi: 10.1071/EN14268
61. Weinberger, F., Freidlander, M., and Gunkel, W. (1994). A bacterial facultative parasite of Gracilaria conferta. Dis. Aquat. Organ. 18, 135-141. doi: 10.3354/dao018135
62. Wilkinson, D., and Ramsdale, M. (2011). Proteases and caspase-like activity in the yeast Saccharomyces cerevisiae. Biochem. Soc. Trans. 39, 1502-1508. doi: 10.1042/BST0391502
63. Wilson, W. H., Tarran, G. A., Schroeder, D., Cox, M., Oke, J., and Malin, G. (2002). Isolation of viruses responsible for the demise of an Emiliania huxleyi bloom in the English Channel. J. Mar. Biol. Assoc. 82, 369-377. doi: 10.1017/S002531540200560X
64. Wilson, W. H., Van Etten, J. L., and Allen, M. J. (2009). The phycodnaviridae: the story of how tiny giants rule the world. Curr. Top. Microbiol. Immunol. 328, 1-42.