Thalassospira sp. isolated from the oligotrophic eastern Mediterranean Sea exhibits chemotaxis toward inorganic phosphate during starvation

Applied and Environmental Microbiology

Volumn 77, Issue 13, 2011, Pages 4412-4421

  Hütz, Annemarie ^a   Schubert, Karin ^a   Overmann, Jörg ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARCHAEON; BACTERIAL PATHOGENS; BACTERIOPLANKTONS; COMPLEX SUBSTRATES; EASTERN MEDITERRANEAN; EASTERN MEDITERRANEAN SEA; GENES CODING; INORGANIC PHOSPHATES; METAGENOMES; NUTRIENT CYCLING; NUTRIENT-LIMITED ENVIRONMENT; ORGANOPHOSPHONATES; PHOSPHATE LIMITATION; PHOSPHATE UPTAKE; PLANKTONIC BACTERIA; PROLONGED STARVATION; PURE CULTURE; WATER COLUMNS; YEAST EXTRACTS;

AMINO ACIDS; BACTERIA; BACTERIOLOGY; CELL CULTURE; GENES; NUTRIENTS; SUGARS;

BIOCHEMISTRY;

AMINO ACID; BACTERIAL DNA; PEPTONE; PHOSPHATE; RIBOSOME DNA; RNA 16S; SEA WATER;

BACTERIOPLANKTON; BACTERIUM; CHEMOTAXIS; GENOME; GROWTH RATE; INORGANIC COMPOUND; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; NUTRIENT CYCLING; NUTRIENT LIMITATION; OLIGOTROPHIC ENVIRONMENT; ORGANOPHOSPHATE; PROKARYOTE; STARVATION; SUGAR; WATER COLUMN;

ARTICLE; CARBOHYDRATE METABOLISM; CHEMISTRY; CHEMOTAXIS; CLUSTER ANALYSIS; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MEDITERRANEAN SEA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; RHODOSPIRILLACEAE;

AMINO ACIDS; CARBOHYDRATE METABOLISM; CHEMOTAXIS; CLUSTER ANALYSIS; DNA, BACTERIAL; DNA, RIBOSOMAL; MEDITERRANEAN SEA; MOLECULAR SEQUENCE DATA; PEPTONES; PHOSPHATES; PHYLOGENY; RHODOSPIRILLACEAE; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA;

MEDITERRANEAN SEA; MEDITERRANEAN SEA (EAST);

ARCHAEA; BACTERIA (MICROORGANISMS); THALASSOSPIRA; THALASSOSPIRA LUCENTENSIS;

EID: 79960098047     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00490-11     Document Type: Article

References (66)

1. Altschul, S. F., et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Azam, F., and F. Malfatti. 2007 Microbial structuring of marine ecosystems. Bacterioplankton growth in the Sargasso Sea. Nat. Rev. Microbiol. 5:782-791.
3. Barbara, G. M., and J. G. Mitchell. 2003. Marine bacterial organisation around point-like sources of amino acids. FEMS Microbiol. Ecol. 43:99-109.
4. Battley, E. H. 1995. An apparent anomaly in the calculation of ash-free dry weights for the determination of cellular yields. Appl. Environ. Microbiol. 61:1655-1657.
5. Braibant, M., and J. Content. 2001. The cell surface associated phosphatase activity of Mycobacterium bovis BCG is not regulated by environmental inorganic phosphate. FEMS Microbiol. Lett. 195:121-126.
6. Cole, J. R., et al. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37:D141-D145.
7. Coolen, M. J. L., and J. Overmann. 2000. Functional exoenzymes as indicators of metabolically active bacteria in 124,000-year-old sapropel layers of the eastern Mediterranean Sea. Appl. Environ. Microbiol. 66:2589-2598.
8. Cotner, J. B., J. W. Ammerman, E. R. Peele, and E. Bentzen. 1997. Phosphorus-limited bacterioplankton growth in the Sargasso Sea. Aquat. Microb. Ecol. 13:141-149.
9. Damoglou, A. P., and E. A. Dawes. 1968. Studies on the lipid content and phosphate requirement of glucose- and acetate-grown Escherichia coli. Biochem. J. 110:775-781.
10. Emeis, K.-C., et al. 2010. External N inputs and internal N cycling traced by isotope ratios of nitrate, dissolved reduced nitrogen, and particulate nitrogen in the eastern Mediterranean Sea. J. Geophys. Res. 115:G04041.
11. Eschemann, A., M. Kühl, and H. Cypionka. 1999. Aerotaxis in Desulfovibrio. Environ. Microbiol. 1:489-494.
12. Feingersch, R., et al. 2010. Microbial community genomics in eastern Mediterranean Sea surface waters. ISME J. 4:78-87.
13. Fröstl, J. M., and J. Overmann. 1998. Physiology and tactic response of the phototrophic consortium "Chlorochromatium aggregatum". Arch. Microbiol. 169:129-135.
14. Fuhrman, J. A., D. E. Comeau, Å. Hagström, and A. M. Chan. 1988. Extraction from natural planktonic microorganisms of DNA suitable for molecular biological studies. Appl. Environ. Microbiol. 54:1426-1429.
15. Fuller, N. J., et al. 2005. Dynamics of community structure and phosphate status of picocyanobacterial populations in the Gulf of Aqaba, Red Sea. Limnol. Oceanogr. 50:363-375.
16. Gebhard, S., N. Ekanayaka, and G. M. Cook. 2009. The low-affinity phosphate transporter PitA is dispensable for in vitro growth of Mycobacterium smegmatis. BMC Microbiol. 9:254.
17. Gich, F., K. Schubert, A. Bruns, H. Hoffelner, and J. Overmann. 2005. Specific detection, isolation and characterization of selected, previously uncultured members of freshwater bacterioplankton. Appl. Environ. Microbiol. 71:5908-5919.
18. Gilbert, J. A., et al. 2009. Potential for phosphonoacetate utilization by marine bacteria in temperate coastal waters. Environ. Microbiol. 11:111-125.
19. Gonin, M., E. M. Quardokus, D. O'Donnol, J. Maddock, and Y. V. Brun. 2000. Regulation of stalk elongation by phosphate in Caulobacter crescentus. J. Bacteriol. 182:337-347.
20. Ikegami, S., I. Imai, J. Kato, and H. Ohtake. 1995. Chemotaxis toward inorganic phosphate in the red tide alga Chattonella antiqua. J. Plankton Res. 17:1587-1591.
21. Janssen, P. H., A. Schuhmann, E. Mörschel, and F. A. Rainey. 1997. Novel anaerobic ultramicrobacteria belonging to the Verrucomicrobiales lineage of bacterial descent isolated by dilution culture from anoxic rice paddy soil. Appl. Environ. Microbiol. 63:1382-1388.
22. Johansen, J. E., J. Pinhassi, N. Blackburn, U. L. Zweifel, and Å. Hagström. 2002. Variability in motility characteristics among marine bacteria. Aquat. Microb. Ecol. 28:229-237.
23. Karl, D. M. 2002. Nutrient dynamics in the deep blue sea. Trends Microbiol. 10:410-418.
24. Kato, J., A. Ito, T. Nikata, and H. Ohtake. 1992. Phosphate taxis in Pseudomonas aeruginosa. J. Bacteriol. 174:5149-5151.
25. Kato, J., Y. Sakai, T. Nikata, and H. Ohtake. 1994. Cloning and characterization of a Pseudomonas aeruginosa gene involved in the negative regulation of phosphate taxis. J. Bacteriol. 176:5874-5877.
26. Kiørboe, T., and G. A. Jackson. 2001. Marine snow, organic solute plumes, and optimal chemosensory behavior of bacteria. Limnol. Oceanogr. 46:1309-1318.
27. Kirkbright, G. F., and M. Marshall. 1973. Direct determination of phosphorus by atomic absorption flame spectrometry. Anal. Chem. 45:1610-1613.
28. Kjelleberg, S., et al. 1993. How do non-differentiating bacteria adapt to starvation? Antonie Van Leeuwenhoek 63:333-341.
29. Kodama, Y., L. I. Stiknowati, A. Ueki, K. Ueki, and K. Watanabe. 2008. Thalassospira tepidiphila sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from seawater. Int. J. Syst. Evol. Microbiol. 58:711-715.
30. Kolowith, L. C., E. D. Ingall, and R. Benner. 2001. Composition and cycling of marine organic phosphorus. Limnol. Oceanogr. 46:309-320.
31. Kusaka, K., K. Shibata, A. Kuroda, J. Kato, and H. Ohtake. 1997. Isolation and characterization of Enterobacter cloacae mutants which are defective in chemotaxis toward inorganic phosphate. J. Bacteriol. 179:6192-6195.
32. Lane, D. J. 1991. 16S/23S rRNA sequencing, p. 115-175. In E. Stackebrandt and M. Goodfellow (ed.), Nucleic acid techniques in bacterial systematics. John Wiley, Chichester, United Kingdom.
33. Liu, C., Y. Wu, L. Li, Y. Ma, and Z. Shao. 2007. Thalassospira xiamenensis sp. nov. and Thalassospira profundimaris sp. nov. Int. J. Syst. Evol. Microbiol. 57:316-320.
34. López-López, A., et al. 2002. Thalassospira lucentensis gen. nov., sp. nov., a new marine member of the α-Proteobacteria. Int. J. Syst. Evol. Microbiol. 52:1277-1283.
35. Ludwig, W., et al. 2004. ARB: a software environment for sequence data. Nucleic Acids Res. 32:1363-1371.
36. Malmcrona-Friberg, K., A. Goodman, and S. Kjelleberg. 1990. Chemotactic responses of marine Vibrio sp. strain S14 CCUG 15956 to low-molecularweight substances under starvation and recovery conditions. Appl. Environ. Microbiol. 56:3699-3704.
37. Manske, A. K., J. Glaeser, M. M. M. Kuypers, and J. Overmann. 2005. Physiology and phylogeny of green sulfur bacteria forming a monospecific phototrophic assemblage at a depth of 100 meters in the Black Sea. Appl. Environ. Microbiol. 71:8049-8060.
38. Martiny, A. C., Y. Huang, and W. Li. 2009. Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environ. Microbiol. 11:1340-1347.
39. Miller, T. R., K. Hnilicka, A. Dziedzic, P. Desplats, and R. Belas. 2004. Chemotaxis of Silicibacter sp. strain TM1040 toward dinoflagellate products. Appl. Environ. Microbiol. 70:4692-4701.
40. Mitchell, J. G., et al. 1995. Long lag times and high velocities in the motility of natural assemblages of marine bacteria. Appl. Environ. Microbiol. 61: 877-882.
41. Navarro Llorens, J. M., A. Tormo, and E. Martínez-García. 2010. Stationary phase in gram-negative bacteria. FEMS Microbiol. Rev. 34:476-495.
42. Neidhardt, F. C., and H. E. Umbarger. 1996. Chemical composition of Escherichia coli, p. 13-16. In F. C. Neidhardt et al. (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. ASM Press, Washington, DC.
43. Ohtake, H., J. Kato, A. Kuroda, H. Wu, and T. Ikeda. 1998. Regulation of bacterial phosphate taxis and polyphosphate accumulation in response to phosphate starvation stress. J. Biosci. 23:491-499.
44. Overmann, J. 2005. Chemotaxis and behavioral physiology of not-yet-cultivated microbes. Methods Enzymol. 397:133-147.
45. Rappé, M. S., S. A. Connon, K. L. Vergin, and S. J. Giovannoni. 2002. Cultivation of the ubiquitous SAR11 marine bacterioplankton clade. Nature 418:630-633.
46. Rubino, A., and D. Hainbucher. 2007. A large abrupt change in the abyssal water masses of the eastern Mediterranean. Geophys. Res. Lett. 34:L23607.
47. Sebastian, M., and J. W. Ammerman. 2009. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J. 3:563-572.
48. Seeger, M., and C. A. Jerez. 1993. Phosphate-starvation induced changes in Thiobacillus ferrooxidans. FEMS Microbiol. Lett. 108:35-41.
49. Smith, D. C., M. Simon, A. L. Alldredge, and F. Azam. 1992. Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359:139-142.
50. Smith, P. K., et al. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150:76-85.
51. Sowell, S. M., et al. 2009. Transport functions dominate the SAR11 metaproteome at low-nutrient extremes in the Sargasso Sea. ISME J. 3:93-105.
52. Stihl, A., U. Sommer, and A. F. Post. 2001. Alkaline phosphatase activities among populations of the colony-forming diazotrophic cyanobacterium Trichodesmium spp. (Cyanobacteria) in the Red Sea. J. Phycol. 37:310-317.
53. Stocker, R., J. R. Seymour, A. Samadani, D. E. Hunt, and M. F. Polz. 2008. Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc. Natl. Acad. Sci. U. S. A. 105:4209-4214.
54. Tanaka, T., et al. 2009. Determining the availability of phosphate and glucose in P-limited mesocosms of NW Mediterranean surface waters. Aquat. Microb. Ecol. 56:81-91.
55. Taniguchi, A., and K. Hamasaki. 2008. Community structures of actively growing bacteria shift along a north-south transect in the western North Pacific. Environ. Microbiol. 10:1007-1017.
56. Tetu, S. G., et al. 2009. Microarray analysis of phosphate regulation in the marine cyanobacterium Synechococcus sp. WH8102. ISME J. 3:835-849.
57. Thingstad, T. F., et al. 2005. Nature of phosphorus limitation in the ultraoligotrophic eastern Mediterranean. Science 309:1068-1071.
58. Van Wambeke, F., U. Christaki, A. Giannakourou, T. Moutin, and K. Souvemerzoglou. 2002. Longitudinal and vertical trends of bacterial limitation by phosphorus and carbon in the Mediterranean Sea. Microb. Ecol. 43:119-133.
59. Wende, A., K. Furtwangler, and D. Oesterhelt. 2009. Phosphate-dependent behavior of the archaeon Halobacterium salinarum strain R1. J. Bacteriol. 191:3852-3860.
60. Willey, J. M., and J. B. Waterbury. 1989. Chemotaxis toward nitrogenous compounds by swimming strains of marine Synechococcus spp. Appl. Environ. Microbiol. 55:1888-1894.
61. Wu, H., et al. 2000. Identification and characterization of two chemotactic transducers for inorganic phosphate in Pseudomonas aeruginosa. J. Bacteriol. 182:3400-3404.
62. Young, C. L., and E. D. Ingall. 2010. Marine dissolved organic phosphorus composition: insights from samples recovered using combined electrodialysis/reverse osmosis. Aquat. Geochem. 16:563-574.
63. Zavaleta-Pastor, M., et al. 2010. Sinorhizobium meliloti phospholipase C required for lipid remodeling during phosphorus limitation. Proc. Natl. Acad. Sci. U. S. A. 107:302.
64. Zohary, T., and R. D. Robarts. 1998. Experimental study of microbial P limitation in the eastern Mediterranean. Limnol. Oceanogr. 43:387-395.
65. Zohary, T., et al. 2005. P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean-a microcosm experiment. Deep Sea Res. Part II Top. Stud. Oceanogr. Stud. Oceanogr. 52:3011-3023.
66. Zubkov, M. V., B. M. Fuchs, H. Eilers, P. H. Burkill, and R. Amann. 1999. Determination of total protein content of bacterial cells by SYPRO staining and flow cytometry. Appl. Environ. Microbiol. 65:3251-3257.