Diel regulation of hydrogen peroxide defenses by open ocean microbial communities

Journal of Plankton Research

Volumn 38, Issue 4, 2016, Pages 1103-1114

  Morris, J Jeffrey ^a,b   Johnson, Zackary I ^c   Wilhelm, Steven W ^d   Zinser, Erik R ^d  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c DUKE UNIVERSITY   (United States)

^d UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Black Queen Hypothesis; Diel; Hydrogen peroxide; Prochlorococcus

Indexed keywords

ANTIBIOTICS; BACTERIUM; BIODEGRADATION; CONCENTRATION (COMPOSITION); DIEL VARIATION; ENZYME; ENZYME ACTIVITY; EUKARYOTE; HYDROGEN PEROXIDE; HYPOTHESIS TESTING; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; OPEN OCEAN; PHYLOGENETICS;

PACIFIC OCEAN; PACIFIC OCEAN (SOUTH);

ALGAE; BACTERIA (MICROORGANISMS); EUKARYOTA; PROCHLOROCOCCUS;

EID: 85040818281     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbw016     Document Type: Article

References (56)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J. H., Zhang, Z., Miller, W. and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
2. Asada, K. (1999) The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 601-639.
3. Avery, G. B. J., Cooper, W. J., Kieber, R. J. and Willey, J. D. (2005) Hydrogen peroxide at the Bermuda Atlantic Time Series Station: Temporal variability of seawater hydrogen peroxide. Mar. Chem., 97, 236-244.
4. Brum, J. R., Morris, J. J., Decima, M. and Stukel, M. R. (2014) Mortality in the Oceans: Causes and Consequences. In: Kemp, P. F. (ed.), Eco-DAS IX Symposium Proceedings. ASLO, pp. 16-48.
5. Cooper, W. J. and Lean, D. R. S. (1989) Hydrogen peroxide concentration in a northern lake: Photochemical formation and diel variability. Environ. Sci. Technol., 23, 1425-1428.
6. Cooper, W. J. and Zepp, R. G. (1990) Hydrogen peroxide decay in waters with suspended soils: Evidence for biologically mediated processes. Can. J. Fish. Aquat. Sci., 47, 888-893.
7. Cooper, W. J., Zika, R. G., Petasne, R. G. and Plane, J. M. C. (1988) Photochemical formation of H2O2 in natural waters exposed to sunlight. Environ. Sci. Technol., 22, 1156-1160.
8. Dufresne, A., Garczarek, L. and Partensky, F. (2005) Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol., 6, R14.
9. Edgar, R. C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
10. Estrela, S., Morris, J. J. and Kerr, B. (2015) Private benefits and metabolic conflicts shape the emergence of microbial interdependencies. Environ. Microbiol. doi:10.1111/1462-2920.13028.
11. Evans, S. N. and Matsen, F. A. (2011) The phylogenetic Kantorovich-Rubinstein metric for environmental sequence samples. arXiv: 1005.1699 [q-bio.PE].
12. Evans, C., Malin, G., Mills, G. P. and Wilson, W. H. (2006) Viral infection of Emiliana huxleyi (Prymnesiophyceae) leads to elevated production of reactive oxygen species. J. Phycol., 42, 1040-1047.
13. Gilbert, J. A., Field, D., Swift, P., Thomas, S., Cummings, D., Temperton, B., Weynberg, K., Huse, S. et al. (2010) The taxonomic and functional diversity of microbes at a temperate coastal site: A 'multi-omic' study of seasonal and diel temporal variation. PLoS One, 5, e15545.
14. Giovannoni, S. J., Tripp, H. J., Givan, S., Podar, M., Vergin, K. L., Baptista, D., Bibbs, L., Eads, J. et al. (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science, 309, 1242-1245.
15. Goldstone, J. V., Pullin, M. J., Bertilsson, S. and Voelker, B. M. (2002) Reactions of hydroxyl radical with humic substances: Bleaching, mineralization, and production of bioavailable carbon substrates. Environ. Sci. Technol., 36, 364-372.
16. Hewson, I., Poretsky, R. S., Tripp, H. J., Montoya, J. P. and Zehr, J. P. (2010) Spatial patterns and light-driven variation of microbial population gene expression in surface waters of the oligotrophic open ocean. Environ. Microbiol., 12, 1940-1956.
17. Hunt, D. E., Lin, Y. J., Church, M. J., Karl, D. M., Tringe, S. G., Izzo, L. K. and Johnson, Z. I. (2013) Relationship between abundance and specific activity of bacterioplankton in open ocean surface waters. Appl. Environ. Microbiol., 79, 177-184.
18. Imlay, J. A. (2003) Pathways of oxidative damage. Annu. Rev. Microbiol., 57, 395-418.
19. Johnson, Z. I., Shyam, R., Ritchie, A. E., Lin, Y., Mioni, C., Lance, V. P., Murray, J. W. and Zinser, E. R. (2010) The effects of iron- and light-limitation on phytoplankton communities of deep chlorophyll maxima of theWestern Pacific Ocean. J. Mar. Res., 68, 1-26.
20. Kanehisa, M. and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res., 28, 27-30.
21. Kieber, R. J., Cooper, W. J., Willey, J. D. and Avery, G. B. Jr. (2001) Hydrogen peroxide at the Bermuda Atlantic Time Series Station. Part 1: Temporal variability of atmospheric hydrogen peroxide and its influence on seawater concentrations. J. Atmos. Chem., 39, 1-13.
22. King, D. W., Cooper, W. J., Rusak, S. A., Peake, B. M., Kiddle, J. J., O'Sullivan, D. W., Melamed, M. L., Morgan, C. R. et al. (2007) Flow injection analysis of H2O2 in natural waters using acridinium ester chemiluminescence: Method development and optimization using a kinetic model. Anal. Chem., 79, 4169-4176.
23. Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K. and Schloss, P. D. (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol., 79, 5112-5120.
24. Lenski, R. E. and Hattingh, S. E. (1986) Coexistence of two competitors on one resource and one inhibitor - a chemostat model based on bacteria and antibiotics. J. Theor. Biol., 122, 83-93.
25. Lin, Y., Gazsi, K., Lance, V. P., Larkin, A. A., Chandler, J. W., Zinser, E. R. and Johnson, Z. I. (2013) In situ activity of a dominant Prochlorococcus ecotype (eHL-II) from rRNA content and cell size. Environ. Microbiol., 15, 2736-2747.
26. Marie, D., Partensky, F., Jacquet, S. and Vaulot, D. (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl. Environ. Microbiol., 63, 186-193.
27. Matsen, F. A., Kodner, R. B. and Armbrust, E. V. (2010) pplacer: Linear time maximum-likelihood and Bayesian phylogenetic placement of sequences onto a fixed reference tree. BMC Bioinformatics, 11, 538.
28. Moffett, J. W. and Zafiriou, O. C. (1990) An investigation of hydrogen peroxide chemistry in surface waters of Vineyard Sound with H2 18O2. Limnol. Oceanogr., 35, 1221-1229.
29. Morris, J. J. (2015) Black Queen evolution: The role of leakiness in structuring microbial communities. Trends Genet., 31, 475-482.
30. Morris, J. J., Kirkegaard, R., Szul, M. J., Johnson, Z. I. and Zinser, E. R. (2008) Facilitation of robust growth of Prochlorococcus colonies and dilute liquid cultures by "helper" heterotrophic bacteria. Appl. Environ. Microbiol., 74, 4530-4534.
31. Morris, J. J., Johnson, Z. I., Szul, M. J., Keller, M. and Zinser, E. R. (2011) Dependence of the cyanobacterium Prochlorococcus on hydrogen peroxide scavenging microbes for growth at the ocean's surface. PLoS One, 6, e16805.
32. Morris, J. J., Lenski, R. E. and Zinser, E. R. (2012) The Black Queen Hypothesis: Evolution of dependencies through adaptive gene loss. mBio, 3, e00036-12.
33. Morris, J. J., Papoulis, S. E. and Lenski, R. E. (2014) Coexistence of evolving bacteria stabilized by a shared Black Queen function. Evolution, 68, 2960-2971.
34. Obernosterer, I., Ruardij, P. and Herndl, G. J. (2001) Spatial and diurnal dynamics of dissolved organic matter (DOM) fluorescence and H2O2 and the photochemical oxygen demand of surface water DOM across the subtropical Atlantic Ocean. Limnol. Oceanogr., 46, 632-643.
35. Ottesen, E. A., Young, C. R., Eppley, J. M., Ryan, J. P., Chavez, F. P., Scholin, C. A. and Delong, E. F. (2013) Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc. Natl Acad. Sci. U.S.A., 110, E488-E497.
36. Ottesen, E. A., Young, C. R., Gifford, S. M., Eppley, J. M., Marin, R., Schuster, S. C., Scholin, C. A. and Delong, E. F. (2014) Multispecies diel transcriptional oscillations in open ocean heterotrophic bacterial assemblages. Science, 345, 207-212.
37. Palenik, B., Zafiriou, O. C. and Morel, F. M. M. (1987) Hydrogen peroxide production by a marine phytoplankter. Limnol. Oceanogr., 32, 1365-1369.
38. Petasne, R. G. and Zika, R. G. (1997) Hydrogen peroxide lifetimes in south Florida coastal and offshore waters. Mar. Chem., 56, 215-225.
39. Poretsky, R. S., Hewson, I., Sun, S., Allen, A. E., Zehr, J. P. and Moran, M. A. (2009) Comparative day/night metatranscriptomic analysis of microbial communities in the North Pacific subtropical gyre. Environ. Microbiol., 11, 1358-1375.
40. Raftery, A. E. (1995) Bayesian model selection in social research. Sociol. Methodol., 25, 111-163.
41. Sachs, J. L. and Hollowell, A. C. (2012) The origins of cooperative bacterial communities. mBio, 3, e00099-12.
42. Scanlan, D. J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., Hess, W. R., Post, A. F., Hagemann, M. et al. (2009) Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev., 73, 249-299.
43. Schloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., Lesniewski, R. A., Oakley, B. B. et al. (2009) Introducing mothur: Open-source, platform-independent, communitysupported software for describing and comparing microbial communities. Appl. Environ. Microbiol., 75, 7537-7541.
44. Schmieder, R., Lim, Y. W. and Edwards, R. (2012) Identification and removal of ribosomal RNA sequences from metatranscriptomes. Bioinformatics, 28, 433-435.
45. Seaver, L. C. and Imlay, J. A. (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J. Bacteriol., 183, 7182-7189.
46. Sokal, R. R. and Rohlf, J. F. (2012) Biometry. Freeman, New York, NY.
47. Southworth, B. A. and Voelker, B. M. (2003) Hydroxyl radical production via the photo-Fenton reaction in the presence of fulvic acid. Environ. Sci. Technol., 37, 1130-1136.
48. Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312-1313.
49. Storz, G., Tartaglia, L. A. and Ames, B. N. (1990) Transcriptional regulator of oxidative stress-inducible genes-direct activation by oxidation. Science, 248, 189-194.
50. Suggett, D. J., Warner, M. E., Smith, D. J., Davey, P., Hennige, S. and Baker, N. R. (2008) Photosynthesis and production of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. J. Phycol., 44, 948-956.
51. Sun, S. L., Chen, J., Li, W. Z., Altintas, I., Lin, A., Peltier, S., Stocks, K., Allen, E. E. et al. (2011) Community cyberinfrastructure for advanced microbial ecology research and analysis: The CAMERA resource. Nucleic Acids Res., 39, D546-D551.
52. Vaulot, D., Courties, C. and Partensky, F. (1989) A simple method to preserve oceanic phytoplankton for flow cytometric analyses. Cytometry, 10, 629-635.
53. Vermilyea, A. W., Hansard, S. P. and Voelker, B. M. (2010) Dark production of hydrogen peroxide in the Gulf of Alaska. Limnol. Oceanogr., 55, 580-588.
54. Yuan, J. and Shiller, A. M. (2001) The distribution of hydrogen peroxide in the southern and central Atlantic ocean. Deep-Sea Res., 48, 2947-2970.
55. Zika, R. G., Saltzman, E. S. and Cooper, W. J. (1985) Hydrogen peroxide concentrations in the Peru upwelling area. Mar. Chem., 17, 265-275.
56. Zinser, E. R., Lindell, D., Johnson, Z. I., Futschik, M. E., Steglich, C., Coleman, M. L.,Wright, M. A., Rector, T. et al. (2009) Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLoS One, 4, e5135.