Effects of phosphorus starvation versus limitation on the marine cyanobacterium ProchlorococcusMED4 II: Gene expression

Environmental Microbiology

Volumn 15, Issue 7, 2013, Pages 2129-2143

  Reistetter, Emily Nahas ^a   Krumhardt, Kristen ^b   Callnan, Kate ^b   Roache Johnson, Kathryn ^b   Saunders, Jaclyn K ^a   Moore, Lisa R ^b   Rocap, Gabrielle ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF SOUTHERN MAINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL MARKER; PHOSPHATE; PHOSPHORUS; PORIN;

ARTICLE; BACTERIAL GENOME; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROCHLOROCOCCUS; SEA;

BACTERIAL PROTEINS; BIOLOGICAL MARKERS; CLUSTER ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; OCEANS AND SEAS; PHOSPHATES; PHOSPHORUS; PORINS; PROCHLOROCOCCUS;

BACTERIA (MICROORGANISMS); PROCHLOROCOCCUS;

EID: 84880037007     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12129     Document Type: Article

References (56)

1. Behrenfeld, M.J., O'Malley, R.T., Siegel, D.A., McClain, C.R., Sarmiento, J.L., Feldman, G.C., etal. (2006) Climate-driven trends in contemporary ocean productivity. Nature 444: 752-755.
2. Bertilsson, S., Berglund, O., Karl, D.M., and Chisholm, S.W. (2003) Elemental composition of marine Prochlorococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol Oceanogr 48: 1721-1731.
3. Bjorkman, K., Thomson-Bulldis, A.L., and Karl, D.M. (2000) Phosphorus dynamics in the North Pacific subtropical gyre. Aquat Microb Ecol 22: 185-198.
4. Bustin, S.A. (2000) Quantification of mRNA using real-time reverse transcription PCR (RT PCR): trends and problems. J Mol Endocrinol 29: 23-39.
5. Coleman, M.L., and Chisholm, S.W. (2010) Ecosystem-specific selection pressures revealed through comparative population genomics. Proc Natl Acad Sci USA 43: 18634-18639.
6. Dehal, P.S., Joachimiak, M.P., Price, M.N., Bates, J.T., Baumohl, J.K., Chivian, D., etal. (2009) MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res 38 (Database issue): D396-D400. doi:10.1093/nar/gkp919.
7. Eisen, M.B., Spellman, P.T., Brown, P.O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868.
8. Finn, R.D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J., etal. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
9. Fuller, N.J., West, N.J., Marie, D., Yallop, M., Rivlin, T., Post, A.F., and 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.
10. Garcia-Fernandez, J.M., Hess, W.R., Houmard, J., and Partensky, F. (1998) Expression of the psbA Gene in the Marine Oxyphotobacteria Prochlorococcus spp. Archives of Biochemistry and Biophysics 359: 17-23.
11. Güler, S., Seeliger, A., Hartel, H., Renger, G., and Benning, C. (1996) A null mutant of Synechococcus sp PCC7942 deficient in the sulfolipid sulfoquinovosyl diacylglycerol. J Biol Chem 271: 7501-7507.
12. Hagio, M., Gombos, Z., Varkonyi, Z., Masamoto, K., Sato, N., Tsuzuki, M., and Wada, H. (2000) Direct evidence for requirement of phosphatidylglycerol in photosystem II of photosynthesis. Plant Physiol 124: 795-804.
13. Heldal, M., Scalan, D.J., Norland, S., Thingstad, F., and Mann, N.H. (2003) Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol Oceanogr 48: 1732-1743.
14. Holtzendorff, J., Partensky, F., Jacquet, S., Bruyant, F., Marie, D., Garczarek, L., etal. (2001) Diel expression of cell cycle-related genes in synchronized cultures of Prochlorococcus sp. strain PCC 9511. J Bacteriol 183: 915-920.
15. de Hoon, M.J.L., Imoto, S., Nolan, J., and Miyano, S. (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
16. Jameson, E., Joint, I., Mann, N.H., and Muhling, M. (2008) Application of a novel rpoC1-RFLP approach reveals that marine Prochlorococcus populations in the Atlantic gyres are composed of greater microdiversity than previously described. Microb Ecol 55: 141-151.
17. Karl, D.M. (1999) A sea of change: biogeochemical variability in the North Pacific Subtropical Gyre. Ecosystems 2: 181-214.
18. Karl, D.M. (2007) The marine phosphorus cycle. In Manual of Environmental Microbiology, 3rd edn. Hurst, C.J., Crawford, R.L., Garland, J.L., Lipson, D.A., Mills, A.L., and Stetzenbach, L.D. (eds). American Society of Microbiology Press: Washington, DC, USA, pp. 523-539.
19. Kathuria, S., and Martiny, A.C. (2011) Prevalence of a calcium-based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Environ Microbiol 13: 74-83.
20. Kettler, G.C., Martiny, A.C., Huang, K., Zucker, J., Coleman, M.L., Rodrigue, S., etal. (2007) Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genet 12: e231.
21. Korteland, J., Tommassen, J., and Lugtenberg, B. (1982) phoE protein pore of the outer membrane of Escherichia coli K12 is a particularly efficient channel for organic and inorganic phosphate. Biochim Biophys Acta 690: 282-289.
22. Krumhardt, K., Callnan, K., Roache-Johnson, K., Swett, T., Robinson, D., Nahas Reistetter, E., etal. (2013) Effects of phosphorus starvation versus limitation on the marine cyanobacterium Prochlorococcus MED4 I: uptake physiology. Environ Microbiol. doi: 10.1111/1462-2920.12079.
23. Lindell, D., and Post, A.F. (2001) Ecological aspects of ntcA gene expression and its use as an indicator of the nitrogen status of marine Synechococcus spp. Appl Environ Microbiol 67: 3340-3349.
24. Lindell, D., Jaffe, J.D., Coleman, M.L., Futschik, M.E., Axmann, I.M., Rector, T., etal. (2007) Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 449: 83-86.
25. Lomas, M.W., Burke, A.L., Lomas, D.A., Bell, D.W., Shen, C., Dyhrman, S.T., and Ammerman, J.W. (2010) Sargasso Sea phosphorus biogeochemistry: an important role for dissolved organic phosphorus (DOP). Biogeosciences 7: 695-710.
26. Martiny, A.C., Coleman, M.L., and Chisholm, S.W. (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103: 12552-12557.
27. Martiny, A.C., Huang, Y., and Weizhong, L. (2009) Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environ Microbiol 11: 1340-1347.
28. Mather, R.L., Reynolds, S.E., Wolff, G.A., Williams, R.G., Torres-Valdes, S., Woodward, E.M.S., etal. (2008) Phosphorus cycling in the North and South Atlantic Ocean subtropical gyres. Nat Geosci 1: 439-443.
29. Moore, L.R., and Chisholm, S.W. (1999) Photophysiology of the marine cyanobacterium Prochlorococcus: ecotypic differences among cultured isolates. Limnol Oceanogr 44: 628-638.
30. Moore, L.R., Rocap, G., and Chisholm, S.W. (1998) Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 393: 464-467.
31. Moore, L.R., Ostrowski, M., Scanlan, D.J., Feren, K., and Sweetsir, T. (2005) Ecotypic variation in phosphorus-acquisition mechanisms within marine picocyanobacteria. Aquat Microb Ecol 39: 257-269.
32. Moore, L.R., Coe, A., Zinser, E.R., Saito, M.A., Sullivan, M.B., Lindell, D., etal. (2007) Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr Methods 5: 353-362.
33. Ostrowski, M., Mazard, S., Tetu, S.G., Phillippy, K., Johnson, D., Palenik, B.P., etal. (2010) PtrA is required for coordinate regulation of gene expression during phosphate stress in a marine Synechococcus. ISME J 4: 908-921.
34. Partensky, F., Hess, W.R., and Vaulot, D. (1999) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127.
35. Ramakers, C., Ruijter, J.M., Deprez, R.H., and Moorman, A.F. (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
36. Rocap, G., Distel, D., Waterbury, J.B., and 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.
37. Rocap, G., Larimer, F.W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N.A., etal. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
38. Rosenberg, H., Gerdes, R.G., and Chegwidden, K. (1977) Two systems for the uptake of phosphate in Escherichia coli. J Bacteriol 131: 505-511.
39. Saier, M.H., Yen, M.R., Noto, K., Tamang, D.G., and Elkan, C. (2009) The Transporter Classification Database: recent advances. Nucleic Acids Res 37: D274-D278.
40. Saldanha, A.J. (2004) Java Treeview - extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
41. Scanlan, D.J., Mann, N.H., and Carr, N.G. (1993) The response of the picoplanktonic marine cyanobacterium Synechococcus species WH7803 to phosphate starvation involves a protein homologous to the periplasmic phosphate-binding protein of Escherichia coli. Mol Microbiol 10: 181-191.
42. Scanlan, D.J., Silman, N.J., Donald, K.M., Wilson, W.H., Carr, N.G., Joint, I., and Mann, N.H. (1997a) An immunological approach to detect phosphate stress in populations and single cells of photosynthetic picoplankton. Appl Environ Microbiol 63: 2411-2420.
43. Scanlan, D.J., Bourne, J.A., and Mann, N.H. (1997b) A putative transcriptional activator of the Crp/Fnr family from the marine cyanobacterium Synechococcus sp. WH7803. J Appl Phycol 8: 565-567.
44. Scanlan, D.J., Ostrowski, M., Mazard, S., Dufresne, A., Garczarek, L., and Hess, W.R. (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73: 249-299.
45. Sebastian, M., and Ammerman, J.W. (2009) The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J 3: 563-572.
46. Shoemaker, J.P., Garland, C.W., and Steinfeld, J.I. (1974) Experiments in Physical Chemistry. New York: McGraw-Hill, pp. 34-39.
47. Su, Z., Olman, V., and Xu, Y. (2007) Computational prediction of Pho regulons in cyanobacteria. BMC Genomics 8: 1-12.
48. Sullivan, M.B., Coleman, M.L., Weigele, P., Rohwer, F., and Chisholm, S.W. (2005) Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol 3: 790-806.
49. Tetu, S.G., Brahamsha, B., Johnson, D.A., Tai, V., Phillippy, K., Palenik, B., and Paulsen, I.T. (2009) Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp WH8102. ISME J 3: 835-849.
50. Toledo, G., and Palenik, B. (1997) Synechococcus diversity in the California Current as seen by RNA polymerase (rpoC1) gene sequences of isolated strains. Appl Environ Microbiol 63: 4298-4303.
51. Tsirigos, K.D., Bagos, P.G., and Hamodrakas, S.J. (2011) OMPdb: a database of beta-barrel outer membrane proteins from Gram-negative bacteria. Nucleic Acids Res 39: D234-D331.
52. Van Mooy, B.A.S., Rocap, G., Fredricks, H.F., Evans, C.T., and Devol, A.H. (2006) Sulfolipids dramatically decrease phosphorus demand by picocyanobacteria in oligotrophic marine environments. Proc Natl Acad Sci USA 103: 8607-8612.
53. Van Mooy, B.A.S., Fredricks, H.F., Pedler, B.E., Dyhrman, S.T., Karl, D.M., Koblížek, M., etal. (2009) Phytoplankton in the ocean substitute lipids in response to phosphorus scarcity. Nature 458: 69-72.
54. Wylie, J.L., and Worobec, E.A. (1995) The OprB porin plays a central role in carbohydrate uptake in Pseudomonas aeruginosa. J Bacteriol 177: 3021-3026.
55. Zeng, Q., and Chisholm, S.W. (2012) Marine viruses exploit their host's two-component regulatory system in response to resource limitation. Curr Biol 22: 124-128.
56. Zinser, E.R., Lindell, D., Johnson, Z.I., Futschik, M.E., Steglich, C., Coleman, M.L., etal. (2009) Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLoS ONE 4: e5135.