Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes

Environmental Microbiology

Volumn 10, Issue 1, 2008, Pages 147-161

  Zwirglmaier, Katrin ^a   Jardillier, Ludwig ^a   Ostrowski, Martin ^a   Mazard, Sophie ^a   Garczarek, Laurence ^b   Vaulot, Daniel ^b   Not, Fabrice ^b,c   Massana, Ramon ^c   Ulloa, Osvaldo ^d   Scanlan, Dave J ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b STATION BIOLOGIQUE DE ROSCOFF   (France)

^c INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^d UNIVERSITY OF CONCEPCIÓN   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S; SEA WATER;

ARTICLE; ECOSYSTEM; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; MOLECULAR GENETICS; MULTIVARIATE ANALYSIS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROCHLOROCOCCUS; SEA; SYNECHOCOCCUS;

BASE SEQUENCE; ECOSYSTEM; GEOGRAPHY; MOLECULAR SEQUENCE DATA; MULTIVARIATE ANALYSIS; OCEANS AND SEAS; PHYLOGENY; PROCHLOROCOCCUS; RNA, RIBOSOMAL, 16S; SEAWATER; SYNECHOCOCCUS; VARIATION (GENETICS);

CYANOBACTERIA; PROCHLOROCOCCUS; SYNECHOCOCCUS;

EID: 38149140067     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2007.01440.x     Document Type: Article

References (54)

1. Ahlgren, N.A. Rocap, G. (2006a) Culture isolation and culture-independent clone libraries reveal new ecotypes of marine Synechococcus with distinctive light and N physiologies. Appl Environ Microbiol 72 : 7193 7204.
2. Ahlgren, N.A., Rocap, G. Chisholm, S.W. (2006b) Measurement of Prochlorococcus ecotypes using real-time polymerase chain reaction reveals different abundances of genotypes with similar light physiologies. Environ Microbiol 8 : 441 454.
3. Borcard, D., Legendre, P. Drapeau, P. (1992) Partialling out the spatial component of ecological variation. Ecology 73 : 1045 1055.
4. Bouman, H.A., Ulloa, O., Scanlan, D.J., Zwirglmaier, K., Li, W.K.W., Platt, T., et al. (2006) Oceanographic basis of the global surface distribution of Prochlorococcus ecotypes. Science 312 : 918 921.
5. Brown, M.V., Schwalbach, M.S., Hewson, I. Fuhrman, J.A. (2005) Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity: development and application to a time series. Environ Microbiol 7 : 1466 1479.
6. Chisholm, S.W., Olson, R.J., Zettler, E.R., Goericke, R., Waterbury, J.B. Welschmeyer, N.A. (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334 : 340 343.
7. Chisholm, S.W., Frankel, S.L., Goericke, R., Olson, R.J., Palenik, B., Waterbury, J.B., et al. (1992) Prochlorococcus marinus nov. gen. nov. sp. an oxyphototrophic marine prokaryote containing divinyl chlorophyll a and b. Arch Microbiol 157 : 297 300.
8. Dolan, J.R. (2005) Biogeography of aquatic microbes. Aquat Microb Ecol 41 : 39 48.
9. Dufresne, A., Salanoubat, M., Partensky, F., Artiguenave, F., Axmann, I.M., Barbe, V., et al. (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci USA 100 : 10020 10025.
10. Ferris, M.J. Palenik, B. (1998) Niche adaptation in ocean cyanobacteria. Nature 396 : 226 228.
11. Follows, M.J., Dutkiewicz, S., Grant, S. Chisholm, S.W. (2007) Emergent biogeography of microbial communities in a model ocean. Science 315 : 1843 1846.
12. Fuller, N.J., Marie, D., Partensky, F., Vaulot, D., Post, A.F. Scanlan, D.J. (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.
13. Fuller, N.J., West, N.J., Marie, D., Yallop, M., Rivlin, T., Post, A.F. Scanlan, D.J. (2005) Dynamics of community structure and phosphate status of picocyanobacterial populations in the Gulf of Aqaba, Red Sea. Limnol Oceanogr 50 : 363 375.
14. Fuller, N.J., Tarran, G.A., Yallop, M., Orcutt, K.M. Scanlan, D.J. (2006) Molecular analysis of picocyanobacterial community structure along an Arabian Sea transect reveals distinct spatial separation of lineages. Limnol Oceanogr 51 : 2515 2526.
15. Garczarek, L., Dufresne, A., Rousvoal, S., West, N.J., Mazard, S., Marie, D., et al. (2007) High vertical and low horizontal diversity of Prochlorococcus ecotypes in the Mediterranean Sea in summer. FEMS Microbiol Ecol 60 : 189 206.
16. Grob, C., Ulloa, O., Claustre, H., Huot, Y., Alarcón, G. Marie, D. (2007) Contribution of picoplankton to the total particulate organic carbon (POC) concentration in the eastern South Pacific. Biogeosci Discuss 4 : 1 37.
17. Herdman, M., Castenholz, R.W., Iteman, I., Waterbury, J. Rippka, R. (2001) The Archaea and the deeply branching and phototrophic bacteria. Subsection I (formerly Chroococcales, Wettstein 1924, emend. Rippka, Deruelles, Waterbury, Herdman and Stanier 1979). In Bergey's Manual of Systematic Bacteriology, 2nd edn, Vol. 1. Boone, D.R. Castenholz, R.W. (eds). New York, USA : Springer-Verlag, pp. 493 514.
18. Heywood, J.L., Zubkov, M.V., Tarran, G.A., Fuchs, B.M. Holligan, P.M. (2006) Prokaryoplankton standing stocks in oligotrophic gyre and equatorial provinces of the Atlantic Ocean: evaluation of inter-annual variability. Deep Sea Res Part II: Top Stud Oceanogr 53 : 1530 1547.
19. Jardillier, L., Boucher, D., Personnic, S., Jacquet, S., Thénot, A., Sargos, D., et al. (2005) Relative importance of nutrients and mortality factors on prokaryotic community composition in two lakes of different trophic status: microcosm experiments. FEMS Microbiol Ecol 53 : 429 443.
20. Johnson, M.T.J. Stinchcombe, J.R. (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22 : 250 257.
21. Johnson, Z.I., Zinser, E.R., Coe, A., McNulty, N.P., Woodward, E.M.S. Chisholm, S.W. (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science 311 : 1737 1740.
22. Li, W.K.W. (1994) Primary production of prochlorophytes, cyanobacteria, and eucaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol Oceanogr 39 : 169 175.
23. Liu, H., Nolla, H.A. Campbell, L. (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol 12 : 39 47.
24. Longhurst, A. (1995) Seasonal cycles of pelagic production and consumption. Prog Oceanogr 36 : 77 167.
25. Longhurst, A. (2007) Ecological Geography of the Sea, 2nd edn. London, UK : Academic Press.
26. Mann, E.L. Chisholm, S.W. (2000) Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific. Limnol Oceanogr 45 : 1067 1076.
27. Mann, E.L., Ahlgren, N., Moffett, J.W. Chisholm, S.W. (2002) Copper toxicity and cyanobacteria ecology in the Sargasso Sea. Limnol Oceanogr 47 : 976 988.
28. Mann, N.H. (2003) Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol Rev 27 : 17 34.
29. Martiny, J.B.H., Bohannan, B.J.M., Brown, J.H., Colwell, R.K., Fuhrman, J.A., Green, J.L., et al. (2006) Microbial biogeography: putting microorganisms on the map. Nat Rev Microbiol 4 : 102 112.
30. Moore, L.R. Chisholm, S.W. (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol Oceanogr 44 : 628 638.
31. Morel, A., Gentili, B., Claustre, H., Babin, M., Bricaud, A., Ras, J. Tièche, F. (2007) Optical properties of the 'clearest' natural waters. Limnol Oceanogr 52 : 217 229.
32. Muhling, M., Fuller, N.J., Somerfield, P.J., Post, A.F., Wilson, W.H., Scanlan, D.J., et al. (2006) High resolution genetic diversity studies of marine Synechococcus isolates using rpoC1-based restriction fragment length polymorphism. Aquat Microb Ecol 45 : 263 275.
33. Muylaert, K., van der Gucht, K., Vloemans, N., de Meester, L., Gillis, M. Vyverman, W. (2002) Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Appl Environ Microbiol 68 : 4740 4750.
34. Not, F., Massana, R., Latasa, M., Marie, D., Colson, C., Eikrem, W., et al. (2005) Late summer community composition and abundance of photosynthetic picoeukaryotes in Norwegian and Barents Seas. Limnol Oceanogr 50 : 1677 1686.
35. Palenik, B., Brahamsha, B., Larimer, F.W., Land, M., Hauser, L., Chain, P., et al. (2003) The genome of a motile marine Synechococcus. Nature 424 : 1037 1042.
36. Palenik, B., Ren, Q., Dupont, C.L., Myers, G.S., Heidelberg, J.F., Badger, J.H., et al. (2006) Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proc Natl Acad Sci USA 103 : 13555 13559.
37. Partensky, F., Hess, W.R. Vaulot, D. (1999a) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63 : 106 127.
38. Partensky, F., Blanchot, J. Vaulot, D. (1999b) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. In Marine Cyanobacteria. No. spécial 19. Charpy, L. Larkum, A.W.D. (eds). Monaco : Bulletin de l'Institut oceanographique, pp. 457 475.
39. Penno, S., Lindell, D. Post, A.F. (2006) Diversity of Synechococcus and Prochlorococcus populations determined from DNA sequences of the N-regulatory gene ntcA. Environ Microbiol 8 : 1200 1211.
40. Rocap, G., Distel, D.L., Waterbury, J.B. Chisholm, S.W. (2002) Resolution of Prochlorococcus and Synechococcus ecotypes by using 16S-23S ribosomal DNA internal transcribed spacer sequences. Appl Environ Microbiol 68 : 1180 1191.
41. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424 : 1042 1047.
42. Rusch, D.B., Halpern, A.L., Sutton, G., Heidelberg, K.B., Williamson, S., Yooseph, S., et al. (2007) The Sorcerer II global ocean sampling expedition: northwest Atlantic through eastern tropical Pacific. PLoS Biol 5 : e77.
43. Saito, M.A., Moffett, J.W., Chisholm, S.W. Waterbury, J.B. (2002) Cobalt limitation and uptake in Prochlorococcus. Limnol Oceanogr 47 : 1629 1636.
44. Saito, M.A., Rocap, G. Moffett, J.W. (2005) Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol Oceanogr 50 : 279 290.
45. Scanlan, D.J. West, N.J. (2002) Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiol Ecol 40 : 1 12.
46. Sode, K., Oonari, R. Oozeki, M. (1997) Induction of a temperate marine cyanophage by heavy metal. J Mar Biotech 5 : 178 180.
47. Thompson, J.R., Pacocha, S., Pharino, C., Klepac-Ceraj, V., Hunt, D.E., Benoit, J., et al. (2005) Genotypic diversity within a natural coastal bacterioplankton population. Science 307 : 1311 1313.
48. Ting, C.S., Rocap, G., King, J. Chisholm, S.W. (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10 : 134 142.
49. Toledo, G. Palenik, B. (2003) A Synechococcus serotype is found preferentially in surface marine waters. Limnol Oceanogr 48 : 1744 1755.
50. Urbach, E., Scanlan, D.J., Distel, D.L., Waterbury, J.B. Chisholm, S.W. (1998) Rapid diversification of marine picophytoplankton with dissimilar light harvesting structures inferred from sequences of Prochlorococcus and Synechococcus (Cyanobacteria). J Mol Evol 46 : 188 201.
51. Veldhuis, M.J.W., Kraay, G.W., van Bleijswijk, J.D.L. Baars, M.A. (1997) Seasonal and spatial variability in phytoplankton biomass, productivity and growth in the northwestern Indian ocean: the southwest and northeast monsoon, 1992-1993. Deep-Sea Res Part I: Oceanogr Res Pap 44 : 425 449.
52. West, N.J. Scanlan, D.J. (1999) Niche-partitioning of Prochlorococcus populations in a stratified water column in the eastern North Atlantic Ocean. Appl Environ Microbiol 65 : 2585 2591.
53. West, N.J., Schönhuber, W.A., Fuller, N.J., Amann, R.I., Rippka, R., Post, A.F. Scanlan, D.J. (2001) Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides. Microbiology 147 : 1731 1744.
54. Zwirglmaier, K., Heywood, J.L., Chamberlain, K., Woodward, E.M.S., Zubkov, M.V. Scanlan, D.J. (2007) Basin-scale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ Microbiol 9 : 1278 1290.