Fine spatial structure of genetically distinct picocyanobacterial populations across environmental gradients in the Costa Rica Dome

Limnology and Oceanography

Volumn 59, Issue 3, 2014, Pages 705-723

  Gutiérrez Rodríguez, Andrés ^a,c   Slack, Gillian ^a   Daniels, Emy F ^a   Selph, Karen E ^b   Palenik, Brian ^a   Landry, Michael R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF HAWAII   (United States)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84898422481     PISSN: 00243590     EISSN: None     Source Type: Journal    
DOI: 10.4319/lo.2014.59.3.0705     Document Type: Article

References (69)

1. Acinas, S. G., V. Klepac-Ceraj, D. E. Hunt, C. Pharino, I. Ceraj, D. L. Distel, and M. F. Polz. 2004. Fine-scale phylogenetic architecture of a complex bacterial community. Nature 430: 551-554, doi: 10. 1038/nature02649.
2. Ahlgren, N. A., and G. Rocap. 2006. Culture isolation and cultureindependent clone libraries reveal new marine Synechococcus ecotypes with distinctive light and N physiologies. Appl. Environ. Microbiol. 72: 7193-7204, doi: 10. 1128/AEM. 00358-06.
3. Ahlgren, N. A., and G. Rocap. 2012. Diversity and distribution of marine Synechococcus: Multiple gene phylogenies for consensus classification and development of qPCR assays for sensitive measurement of clades in the ocean. Front. Microbiol 3: 1-24, doi: 10. 3389/fmicb. 2012. 00213.
4. Apple, J. K., S. L. Strom, B. Palenik, and B. Brahamsha. 2011. Variability in protist grazing and growth on different marine Synechococcus isolates. Appl. Environ. Microbiol. 77: 3074-3084, doi: 10. 1128/AEM. 02241-10.
5. Barnett, J. P., A. Millard, A. Z. Ksibe, D. J. Scanlan, R. Schmid, and C. A. Blindauer. 2012. Mining genomes of marine cyanobacteria for elements of zinc homeostasis. Front. Microbiol 3: 1-21, doi: 10. 3389/fmicb. 2012. 00142.
6. Baudoux, A. C., M. J. W. Veldhuis, A. A. M. Noordeloos, G. Van Noort, and C. P. D. Brussaard. 2008. Estimates of virus-vs. grazing induced mortality of picophytoplankton in the North Sea during summer. Aquat. Microb. Ecol 52: 69-82, doi: 10. 3354/ame01207.
7. Campbell, L., M. R. Landry, J. Constantinou, H. A. Nolla, S. L. Brown, H. Liu, and D. A. Caron. 1998. Response of microbial community structure to environmental forcing in the Arabian Sea. Deep-Sea Res. II 45: 2301-2325, doi: 10. 1016/S0967-0645(98)00072-1.
8. Casey, J. R., M. W. Lomas, J. Mandecki, and D. E. Walker. 2007. Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum. Geophys. Res. Lett. 34: 1-5.
9. Coleman, M. L., and S. W. Chisholm. 2007. Code and context: Prochlorococcus as a model for cross-scale biology. Trends Microbiol. 15: 398-407, doi: 10. 1016/j. tim. 2007. 07. 001.
10. Collier, J. L., and B. Palenik. 2003. Phycoerythrin-containing picoplankton in the Southern California Bight. Deep-Sea Res. II 50: 2405-2422, doi: 10. 1016/S0967-0645(03)00127-9.
11. Doolittle, D. F., W. K. W. Li, and A. M. Wood. 2008. Wintertime abundance of picoplankton in the Atlantic sector of the Southern Ocean. Nova Hedwigia 133: 147-160.
12. Edgar, R. C. 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792-1797, doi: 10. 1093/nar/gkh340.
13. Ferris, M. J., and B. Palenik. 1998. Niche adaptation in ocean cyanobacteria. Nature 396: 226-228, doi: 10. 1038/24297.
14. Fiedler, P. C. 2002. The annual cycle and biological effects of the Costa Rica Dome. Deep-Sea Res. I 49: 321-338.
15. Fiedler, P. C., and L. D. Talley. 2006. Hydrography of the eastern tropical Pacific: A review. Prog. Oceanogr. 69: 143-180, doi: 10. 1016/j. pocean. 2006. 03. 008.
16. Franck, V., K. Bruland, D. Hutchins, and M. Brzezinski. 2003. Iron and zinc effects on silicic acid and nitrate uptake kinetics in three high-nutrient, low-chlorophyll (HNLC) regions. Mar. Ecol. Prog. Ser. 252: 15-33, doi: 10. 3354/meps252015.
17. Fuller, N. J., D. Marie, D. Vaulot, A. F. Post, and D. J. Scanlan. 2003. Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl. Environ. Microbiol. 69: 2430-2443, doi: 10. 1128/AEM. 69. 5. 2430-2443. 2003.
18. Fuller, N. J., G. A. Tarran, M. Yallop, K. M. Orcutt, and D. J. Scanlan. 2006. Molecular analysis of picocyanobacterial community structure along an Arabian Sea transect reveals distinct spatial separation of lineages. Limnol. Oceanogr. 51: 2515-2526, doi: 10. 4319/lo. 2006. 51. 6. 2515.
19. Goericke, R., R. J. Olson, and A. Shalapyonok. 2000. A novel niche for Prochlorococcus sp. in low-light suboxic environments in theArabian Sea and the Eastern TropicalNorth Pacific. Deep-Sea Res. I 47: 1183-1205, doi: 10. 1016/S0967-0637(99)00108-9.
20. Gutiérrez-Rodríguez, A., M. Latasa, S. Agustí, and C. M. Duarte. 2011. Distribution and contribution of major phytoplankton groups to carbon cycling across contrasting conditions of the subtropical northeast Atlantic Ocean. Deep-Sea Res. I 58: 1115-1129, doi: 10. 1016/j. dsr. 2011. 08. 003.
21. Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological statistics software Package for education and data analysis. Palaeontologia Electronica 4: 1-9 [accessed 29 January 2014]. Available from http://palaeo-electronica. org/2001_1/past/issue1_01. htm.
22. Hou, Y., H. Zhang, L. Miranda, and S. Lin. 2010. Serious overestimation in quantitative PCR by circular (supercoiled) plasmid standard: Microalgal pcna as the model gene. PLoS One 5: e9545, doi: 10. 1371/journal. pone. 0009545.
23. Huang, S., S. W. Wilhelm, H. R. Harvey, K. Taylor, N. Jiao, and F. Chen. 2011. Novel lineages of Prochlorococcus and Synechococcus in the global oceans. ISME J. 6: 285-297, doi: 10. 1038/ismej. 2011. 106.
24. Jardillier, L., M. V. Zubkov, J. Pearman, and D. J. Scanlan. 2010. Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J. 4: 1180-1192, doi: 10. 1038/ismej. 2010. 36.
25. Johnson, Z., and others. 1999. Energetic and growth kinetics of a deep Prochlorococcus population in the Arabian Sea. Deep-Sea Res. II 46: 1719-1743, doi: 10. 1016/S0967-0645(99) 00041-7.
26. Landry, M. R., and D. L. Kirchman. 2002. Microbial community structure and variability in the tropical Pacific. Deep-Sea Res. II 49: 2669-2694, doi: 10. 1016/S0967-0645(02)00053-X.
27. Landry, M. R., M. D. Ohman, R. Goericke, M. R. Stukel, and K. Tsyrklevich. 2009. Lagrangian studies of phytoplankton growth and grazing relationships in a coastal upwelling ecosystem off Southern California. Prog. Oceanogr. 83: 208-216, doi: 10. 1016/j. pocean. 2009. 07. 026.
28. Lavín, P., B. González, J. F. Santibáñez, D. J. Scanlan, and O. Ulloa. 2010. Novel lineages of Prochlorococcus thrive within the oxygen minimum zone of the eastern tropical South Pacific. Environ. Microbiol. Rep. 2: 728-738, doi: 10. 1111/j. 1758-2229. 2010. 00167.
29. Li, W. K. W. 1994. Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: Measurements from flow cytometric sorting. Limnol. Oceanogr. 39: 169-175, doi: 10. 4319/lo. 1994. 39. 1. 0169.
30. Li, W. K. W., D. V. S. Rao, W. G. Harrison, J. C. Smith, J. J. Cullen, B. Irwin, and T. Platt. 1983. Autotrophic picoplankton in the tropical ocean. Science 219: 292-295, doi: 10. 1126/science. 219. 4582. 292.
31. Li, W. K. W., and A. M. Wood. 1988. Vertical distribution of North Atlantic ultraphytoplankton: Analysis by flow cytometry and epifluorescence microscopy. Deep-Sea Res. 35: 1615-1638, doi: 10. 1016/0198-0149(88)90106-9.
32. Martiny, A. C., S. Kathuria, and P. M. Berube. 2009a. Widespread metabolic potential for nitrite and nitrate assimilation among Prochlorococcus ecotypes. Proc. Natl. Acad. Sci. USA 106: 10787-10792, doi: 10. 1073/pnas. 0902532106.
33. Martiny, A. C., A. P. K. Tai, D. Veneziano, F. Primeau, and S. W. Chisholm. 2009b. Taxonomic resolution, ecotypes and the biogeography of Prochlorococcus. Environ. Microbiol. 11: 823-832, doi: 10. 1111/j. 1462-2920. 2008. 01803.
34. Mazard, S., M. Ostrowski, F. Partensky, and D. J. Scanlan. 2012. Multi-locus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus. Environ. Microbiol. 14: 372-386, doi: 10. 1111/j. 1462-2920. 2011. 02514.
35. Moore, L. R., and S. W. Chisholm. 1999. Photophysiology of the marine cyanobacterium Prochlorococcus: Ecotypic differences among cultured isolates. Limnol. Oceanogr. 44: 628-638, doi: 10. 4319/lo. 1999. 44. 3. 0628.
36. Mühling, M., and others. 2005. Genetic diversity of marine Synechococcus and co-occurring cyanophage communities: Evidence for viral control of phytoplankton. Environ. Microbiol. 7: 499-508, doi: 10. 1111/j. 1462-2920. 2005. 00713.
37. Mühling, M., and others. 2006. High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length polymorphism. 2006. Aquat. Microb. Ecol. 45: 263-275, doi: 10. 3354/ame045263.
38. Olson, R. J., S. W. Chisholm, E. R. Zettler, and E. V. Armbrust. 1990. Pigments, size, and distribution of Synechococcus in the North Atlantic and Pacific Oceans. Limnol. Oceanogr. 35: 45-58, doi: 10. 4319/lo. 1990. 35. 1. 0045.
39. Paerl, R. W., K. S. Johnson, R. M. Welsh, A. Z. Worden, F. P. Chavez, and J. P. Zehr. 2011a. Differential distributions of Synechococcus subgroups across the California Current System. Front. Microbiol. 2: 1-22, doi: 10. 3389/fmicb. 2011. 00059.
40. Paerl, R. W., K. A. Turk, R. A. Beinart, F. P. Chavez, and J. P. Zehr. 2011b. Seasonal change in the abundance of Synechococcus and multiple distinct phylotypes in Monterey Bay determined by rbcL and narB quantitative PCR. Environ. Microbiol. 14: 580-593, doi: 10. 1111/j. 1462-2920. 2011. 02594.
41. Palenik, B. 1994. Cyanobacterial community structure as seen from RNA polymerase gene sequence analysis. Appl. Environ. Microbiol. 60: 3212-3219.
42. Palenik, B. 2001. Chromatic adaptation in marine Synechococcus strains. Appl. Environ. Microbiol. 67: 991-994, doi: 10. 1128/AEM. 67. 2. 991.
43. Palenik, B., and others. 2006. Genome sequence of Synechococcus CC9311: Insights into adaptation to a coastal environment. Proc. Natl. Acad. Sci. USA 103: 13555-13559, doi: 10. 1073/pnas. 0602963103.
44. Partensky, F., J. Blanchot, F. Lantoine, J. Neveux, and D. Marie. 1996. Vertical structure of picophytoplankton at different trophic sites of the tropical northeastern Atlantic Ocean. Deep-Sea Res. I 43: 1191-1213, doi: 10. 1016/0967-0637(96)00056-8.
45. Partensky, F., J. Blanchot, and D. Vaulot. 1999. Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters, p. 457-475. In L. C. and A. Larkum [eds.], Marine cyanobacteria. Musee Oceanographique.
46. Partensky, F., and L. Garczarek. 2010. Prochlorococcus: Advantages and limits of minimalism. Ann. Rev. Mar. Sci. 2: 305-331, doi: 10. 1146/annurev-marine-120308-081034.
47. Post, A. F., S. Penno, K. Zandbank, A. S. Paytan, M. Huse, and D. M. Welch. 2011. Long term seasonal dynamics of Synechococcus population structure in the Gulf of Aqaba, northern Red Sea. Front. Microbiol. 2: 1-12, doi: 10. 3389/fmicb. 2011. 00131.
48. Rivers, A. R., R. W. Jakuba, and E. A. Webb. 2009. Iron stress genes in marine Synechococcus and the development of a flow cytometric iron stress assay. Environ. Microbiol. 11: 382-396, doi: 10. 1111/j. 1462-2920. 2008. 01778.
49. Rocap, G., D. L. Distel, J. B. Waterbury, and S. W. Chisholm. 2002. Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl. Environ. Microbiol. 68: 1180-1191, doi: 10. 1128/AEM. 68. 3. 1180.
50. Rocap, G., and others. 2003. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047, doi: 10. 1038/nature01947.
51. Saito, M. A., G. Rocap, and J. W. Moffett. 2005. Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol. Oceanogr. 50: 279-290, doi: 10. 4319/lo. 2005. 50. 1. 0279.
52. Scanlan, D. J., and N. J. West. 2002. Molecular ecology of themarine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol. Rev. 40: 1-12, doi: 10. 1111/j. 1574-6941. 2002. tb00930. x.
53. Scanlan, D. J., and others. 2009. Ecological genomics of marine picocyanobacteria. Microbiol. Mol. Biol. Rev. 73: 249-299, doi: 10. 1128/MMBR. 00035-08.
54. Schlitzer, R. 2006. Ocean Data View [accessed 29 January 2014]. Available from http://odv. awi. de.
55. Selph, K. E., and others. 2011. Spatially-resolved taxon-specific phytoplankton production and grazing dynamics in relation to iron distributions in the Equatorial Pacific between 110 and 140uW. Deep-Sea Res. II 58: 358-377, doi: 10. 1016/j. dsr2. 2010. 08. 014.
56. Stuart, R. K., B. Brahamsha, K. Busby, and B. Palenik. 2013. Genomic islands in a coastal marine Synechococcus strain confer enhanced tolerance to copper and oxidative stress. ISME J. 7: 1139-1149, doi: 10. 1038/ismej. 2012. 175.
57. Tai, V., R. Burton, and B. Palenik. 2011. Temporal and spatial distributions of marine Synechococcus in the Southern California Bight assessed by hybridization to bead-arrays. Mar. Ecol. Prog. Ser. 426: 133-147, doi: 10. 3354/meps09030.
58. Tai, V., and B. Palenik. 2009. Temporal variation of Synechococcus clades at a coastal Pacific Ocean monitoring site. ISME J. 3: 903-915, doi: 10. 1038/ismej. 2009. 35.
59. Tamura, K., and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNAin humans and chimpanzees. Mol. Biol. Evol. 10: 512-526.
60. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. 28: 1530-1534, doi: 10. 1093/molbev/msr121.
61. Taylor, A. G., M. R. Landry, K. E. Selph, and E.-J. Yang. 2011. Biomass, size structure and depth distributions of the microbial community in the eastern equatorial Pacific. Deep-Sea Res. II 58: 342-357, doi: 10. 1016/j. dsr2. 2010. 08. 017.
62. Toledo, G., and B. Palenik. 1997. Synechococcus diversity in the California current as seen by RNA polymerase (rpoC1) gene sequences of isolated strains. Appl. Environ. Microbiol. 63: 4298-4303.
63. Wang, C., and P. C. Fiedler. 2006. ENSO variability and the eastern tropical Pacific: A review. Prog. Oceanogr. 69: 239-266, doi: 10. 1016/j. pocean. 2006. 03. 004.
64. Waterbury, J. B., S. W. Watson, R. R. L. Guillard, and L. E. Brand. 1979. Widespread occurrence of a unicellular, marine, planktonic cyanobacterium. Nature 277: 293-294, doi: 10. 1038/277293a0.
65. Wood, A. M., P. K. Horan, K. Muirhead, D. A. Phinney, C. M. Yentsch, and J. B. Waterbury. 1985. Discrimination between types of pigments in marine Synechococcus spp. by scanning spectroscopy, epifluorescence microscopy, and flow cytometry. Limnol. Oceanogr. 30: 1303-1315, doi: 10. 4319/lo. 1985. 30. 6. 1303.
66. Wyrtki, K. 1964. Upwelling in the Costa Rica Dome. Fish. Bull. 63: 355-372.
67. Zinser, E. R., Z. I. Johnson, A. Coe, D. Veneziano, and S. W. Chisholm. 2007. Influence of light and temperature on Prochlorococcus ecotype distributions in the Atlantic Ocean. Limnol. Oceanogr. 52: 2205-2220, doi: 10. 4319/lo. 2007. 52. 5. 2205.
68. Zwirglmaier, K., J. L. Heywood, K. Chamberlain, E. M. S. Woodward, M. V. Zubkov, and D. J. Scanlan. 2007. Basinscale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ. Microbiol. 9: 1278-1290, doi: 10. 1111/j. 1462-2920. 2007. 01246. x.
69. Zwirglmaier, K., and others. 2008. Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ. Microbiol. 10: 147-161, doi: 10. 1111/j. 1462-2920. 2007. 01440.