Gammaproteobacterial diazotrophs and nifH gene expression in surface waters of the South Pacific Ocean

ISME Journal

Volumn 8, Issue 10, 2014, Pages 1962-1973

  Moisander, Pia H ^a,b   Serros, Tracy ^a   Paerl, Ryan W ^a,c   Beinart, Roxanne A ^a,d   Zehr, Jonathan P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MASSACHUSETTS DARTMOUTH   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

Author keywords

Crocosphaera; diel cycle; nifH; nitrogen cycle; transcription; UCYN A

Indexed keywords

CYANOBACTERIUM; DIEL VARIATION; GENE EXPRESSION; GENETIC VARIATION; NITROGEN CYCLE; SURFACE WATER;

PACIFIC OCEAN; PACIFIC OCEAN (SOUTH);

CROCOSPHAERA; CYANOBACTERIA;

NITROGENASE REDUCTASE; OXIDOREDUCTASE; SEA WATER;

CYANOBACTERIUM; GAMMAPROTEOBACTERIA; GENE DOSAGE; GENE EXPRESSION; GENETICS; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PACIFIC OCEAN; PHYLOGENY; TEMPERATURE;

CYANOBACTERIA; GAMMAPROTEOBACTERIA; GENE DOSAGE; GENE EXPRESSION; NITROGEN FIXATION; OXIDOREDUCTASES; PACIFIC OCEAN; PHYLOGENY; SEAWATER; TEMPERATURE; WATER MICROBIOLOGY;

EID: 84921539168     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.49     Document Type: Article

References (69)

1. Benavides M, Agawin NSR, Aristegui J, Ferriol P, Stal LJ. (2011). Nitrogen fixation by Trichodesmium and small diazotrophs in the subtropical northeast Atlantic. Aquat Microb Ecol 65: 43-53.
2. Bird C, Martinez JM, O'Donnell AG, Wyman M. (2005). Spatial distribution and transcriptional activity of an uncultured clade of plank tonic diazotrophic gammaproteobacteria in the Arabian Sea. Appl Environ Microbiol 71: 2079-2085.
3. Bombar D, Moisander PH, Dippner JW, Foster RA, Voss M, Karfield B et al. (2011). Distribution of diazo trophic microorganisms and nifH gene expression in the Mekong River plume during intermonsoon. Mar Ecol Prog Ser 424: 39-52.
4. Bonnet S, Biegala IC, Dutrieux P, Slemons LO, Capone DG. (2009). Nitrogen fixation in the western equatorial pacific: rates, diazotrophic cyanobacterial size class distribution, and biogeochemical significance. Global Biogeochem Cycl 23: GB3012.
5. Bostrom KH, Riemann L, Kuhl M, Hagstrom A. (2007). Isolation and gene quantification of heterotrophic N-2-fixing bacterioplankton in the Baltic Sea. Environ Microbiol 9: 152-164.
6. Capone DG, Zehr JP, Paerl HW, Bergman B, Carpenter EJ. (1997). Trichodesmium, a globally significant marine cyanobacterium. Science 276: 1221-1229.
7. Carlson CA, Giovannoni SJ, Hansell DA, Goldberg SJ, Vergin K. (2004). Interactions among dissolved organic carbon, microbial processes, and community structure in the mesopelagic zone of the northwestern Sargasso Sea. Limnol Oceanogr 49: 1073-1083.
8. Carpe nter EJ, Montoya JP, Burns J, Mulholland MR, Subramaniam A, Capone DG. (1999). Extensive bloom of a N-2-fixing diatom/cyanobacterial association in the tropical Atlantic Ocean. Mar Ecol Prog Ser 185: 273-283.
9. Chen Y, Zehr JP, Mellon MT. (1996). Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanbacterium Trichodesmium sp. IMS 101 in defined media: evidence for a circadian rhythm. J Phycol 32: 916-923.
10. Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP. (2005). Temporal patterns of nitrogenase gene (nifH) expression in the oligotrophic North Pacific Ocean. Appl Environ Microbiol 71: 5362-5370.
11. Dekaezemacker J Bonnet S. 2011 Sensitivity of N-2 fixation to combined nitrogen forms (NO3-and NH4 ) in two strains of the marine diazotroph Crocosphaera watsonii (Cyanobacteria). Mar Ecol Prog Ser438 33-46.
12. Diez B, Bergman B, Pedros-Alio C, Anto M, Snoeijs P. (2012). High cyanobacterial nifH gene diversity in Arctic seawater and sea ice brine. Environ Microbiol Rep 4: 360-366.
13. Dixon R, Kahn D. (2004). Genetic regulation of biological nitrogen fixation. Nat Rev Microbiol 2: 621-631.
14. Falcon LI, Carpenter EJ, Cipriano F, Bergman B, Capone DG. (2004). N-2 fixation by unicellular bacterioplankton from the Atlantic and Pacific oceans: phylogeny and in situ rates. Appl Environ Microbiol 70: 765-770.
15. Fay P. (1992). Oxygen relations of nitrogen fixatioin in cyanobacteria. Microbiol Rev 56: 340-373.
16. Fong AA, Karl DM, Lukas R, Letelier RM, Zehr JP, ChurchMJ. (2008). Nitrogen fixation in an anticyclonic eddy in the oligotrophic North Pacific Ocean. ISME J 2: 663-676.
17. Foster RA, Paytan A, Zehr JP. (2009). Seasonality of N-2 fixation and nifH gene diversity in the Gulf of Aqaba (Red Sea). Limnol Oceanogr 54: 219-233.
18. Graziano LM, Geider RJ, Li WKW, Olaizola M. (1996). Nitrogen limitation of North Atlantic phytoplankton: analysis of physiological condition in nutri ent enrichment experiments. Aquat Micr Ecol 11: 53-64.
19. Halm H, Lam P, Ferdelman TG, Lavik G, Dittmar T, LaRoche J et al. (2012). Heterotrophic organisms dominate nitrogen fixation in the South P acific Gyre. The ISME J 6: 1238-1249.
20. Hamersley MR, Turk KA, Leinweber A, Gruber N, Zehr JP, Gunderson T et al. (2011). Nitrogen fixation within the water column associated with two hypoxic basins in the Southern California Bight. Aquat Micr Ecol 63: 193-205.
21. Hewson I, Moisander PH, Achilles KM, Carlson CA, Jenkins BD, Mondragon EA et al. (2007). Characteristics of diazotrophs in surface to abyssopelagic waters of the Sargasso Sea. Aquat Micr Ecol 46: 15-30.
22. Johnson ZI, Zinser ER, Coe A, McNulty NP, Woodward M, Chisholm SW. (2006). Niche partitioning among Prochlorococcus ecotype abundances in the North Atlantic Ocean revealed by an improved q uantitative PCR method. Science 311: 1737-1740.
23. Karl D, Letelier R, Tupas L, Dore J, Christian J, Hebel D. (1997). The role of nitrogen fixation in biogeochemical cycling in the subtropical Nort h Pacific Ocean. Nature 388: 533-538.
24. Karl DM, Tien G. (1992). MAGIC: A sensitive and precise method for measuring dissolved phosphorus in aquatic environments. Limnol Oceanogr 37: 105-116.
25. Kirchman DL,Meon B, CottrellMT, Hutchins DA,Weeks D, Bruland KW. (2000). Carbon versus iron limitation of bacterial growth in the California upwelling regime. Limnol Oceanogr 45: 1681-1688.
26. Lan glois RJ, LaRoche J, Raab PA. (2005). Diazotrophic diversity and distribution in the tropical and subtropical Atlantic ocean. Appl Environ Microbiol 71: 7910-7919.
27. Le Moal M, Biegala IC. (2009). Diazotrophic unicellular cyanobacteria in the northwestern Mediterranean Sea: a seasonal cycle. Limnol Oceanogr 54: 845-855.
28. Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar et al. (2004). ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
29. Mahaffey C, Michaels AF, Capone DG. (2005). The conundrum of marine N-2 fixation. Am J Sci 305: 546-595.
30. Man-Aharonovich D, Kress N, Bar Zeev E, Berman-Frank I, Beja O. (2007). Molecular ecology of nifH genes and transcripts in the eastern Mediterranean Sea. Environ Microbiol 9: 2354-2363.
31. Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon R. (2005). Nitrogen fixation: key genetic regulatory mechanisms. Biochem Soc Trans 33(part 1): 152-156.
32. Masuda T Furuya K Koda ma T Takeda S Harrison PJ. 2013 Ammonium uptake and dinitrogen fixation by the unicellular nanocyanobacterium Crocosphaera watsonii in nitrogen-limited continuous cultures. Limnol Oceanogr 58 2029-2036.
33. M ills MM, Ridame C, Davey M, La Roche J, Geider RJ. (2004). Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic. Nature 429: 292-294.
34. Moisander PH, Beinart RA, Hewson I, White AE, Johnson KS, Carlson CA et al. (2010). Unicellular cyanobacterial distributions broaden the oceanic N-2 fixation domain. Science 327: 1512-1514.
35. Moisander PH, Beinart RA, Voss M, Zehr JP. (2008). Diversity and abundance of diazotrophic microorganisms in the South China Sea during intermonsoon. ISME J 2: 954-967.
36. Moisander PH, Zhang R, Boyle EA, Hewson I, Montoya JP, Zehr JP. (2011). Analogous nutrient limitations in unicellular diazotrophs and Prochlorococcus in the South Pacific Ocean. ISME J 6: 733-744.
37. Montoya JP, Holl CM, Zeh r JP, Hansen A, Villareal TA, Capone DG. (2004). High rates of N-2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature 430: 1027-1031.
38. Oelze J. (2000). Respiratory pro tection of nitrogenase in Azotobacter species: is a widely held hypothesis unequivocally supported by experimental evidence? FEMS Microbiol Rev 24: 321-333.
39. Omoregie EO, Crumbliss LL, Bebout BM, Zehr JP. (2004). Determination of nitrogen-fixing phylotypes in Lyngbya sp and Microcoleus chthonoplastes cyanobacterial mats from Guerrero Negro, Baja California, Mexico. Appl Environ Microbiol 70: 2119-2128.
40. Ottesen EA, Young CR, Eppley JM, Ryan JP, Chavez FP, Scholin CA et al. (2013). Pattern and synchrony of gene expression among sympatric marine microbial populations. Proc Natl Acad Sci USA 110: E488-E497.
41. Postgate J (ed). (1990). Nitrogen fixation, Second edition Edward Arnold: Great Britain.
42. Rabouille S, Staal M, Stal LJ, Soetaert K. (2006). Modeling the dynamic regulation of nitrogen fixation in the cyanobacterium Trichodesmium sp. Appl Environ Microbiol 72: 3217-3227.
43. Rediers H, Vanderleyden J, De Mot R. (2004). Azotobacter vinelandii: a Pseudomonas in disguise? Microbiology 150: 1117-1119.
44. Sakamoto C M, Friederich GE, Codispoti LA. (1990). MBARI Procedures for Automated Nutrient Analyses Using a Modified Alpkem Series 300 Rapid Flow Analyzer. Monteray Bay Aquarium Research Institute.
45. Shi T, Ilikchyan I, Rabouille S, Zehr JP. (2010). Genomewide analysis of diel gene expression in the unicellular N-2-fixing cyanobacterium Crocosphaera watsonii WH 8501. ISME J 4: 621-632.
46. Short SM, Zehr JP. (2005). Qua ntitative analysis of nifH genes and transcripts from aquatic environments. Meth Enzymol 397: 380-394.
47. Short SM, Zehr JP. (2007). Nitrogenase gene expression in the Chesapeake Bay Estuary. Environ Microbiol 9: 1591-1596.
48. Soriano M, Roibas B, Garcia AB, Espinosa-Urgel M. (2010). Evidence of circadian rhythms in non-photosynthetic bacteria? J Circadian Rhythms 8: 8.
49. Staal M, Hekkert StL, Brummer GJ, Veldhuis M, Sikkens C, Persijn S et al. (2007a ). Nitrogen fixation along a north-south transect in the eastern Atlantic Ocean. Limnol Oceanogr 52: 1305-1316.
50. Staal M, Rabouille S, Stal LJ. (2007b ). On the role of oxygen for nitrogen fixation in the marine cyanobacterium Trichodesmium sp. Environ Microbiol 9: 727-736.
51. Strickland JDH, Parsons TR. (1972). A Practical Handbook Of Seawater Analysis. Bulletin 167, 2nd edn. Fisheries Reserach Board Ottawa: Canada.
52. Thingstad TF, Bellerby RGJ, Bratbak G, Borsheim KY, Egge JK , Heldal M et al. (2008). Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455: 387-U337.
53. Thompson AW Foster R.A. Krupke A Carter BJ Musat NM Vaulot D et al . 2012 Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337 1546-1550.
54. Treusch AH, Vergin KL, Finlay LA, Donatz MG, Burton RM, Carlson CA et al. (2009 ). Seasonality and vertical structure of microbial communities in an ocean gyre. ISME J 3: 1148-1163.
55. Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F et al. (2010). Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium. Nature 464: 90-94.
56. Tuit C, Waterbury J, Ravizzaz G. (2004). Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnol Oceanogr 49: 978-990.
57. Turk KA, Rees AP, Zehr JP, Pereira N, Swift P, Shelley R et al. (2011). Nitrogen fixation and nitrogenase (nifH) expression in tropical waters of the eastern North Atlantic. IS ME J 5: 1201-1212.
58. Villareal TA. (1994). Widespread occurrence of the Hemiaulus-cyanobacterial symbiosis in the southwest North Atlantic ocean. Bull Mar Sci 54: 1-7.
59. Walsh TW. (1989) . Total dissolved nitrogen in seawater: A new high combustion method and a comparison to photo-oxidation. Mar Chem 26: 295-311.
60. Welschmeyer NA. (1994). Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39: 1985-1992.
61. Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi Tet al. (2008). Globally distributed uncultivated oceanic N-2-Fixing Cyanoba cteria lack Oxygenic Photosystem II. Science 322: 1110-1112.
62. Zehr JP, Crumbliss LL, Church MJ, Omoregie EO, Jenkins BD. (2003a ). Nitrogenase genes in PCR and RT-PCR reagents: implications for studies of diversity of functional genes. Biotechniques 35: 996-1002.
63. Zehr JP, Jenkins BD, Short SM, Steward GF. (2003b ). Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5: 539-554.
64. Zehr JP, Kudela RM. (2011). Nitrogen Cycle of the Open Ocean: From Genes to Ecosystems 197-225. in Carlson CA, Giovannoni SJ (eds). Annual R eview of Marine Science, Vol 3. Annual Reviews: Palo Alto, CA, USA.
65. Zehr JP, Mellon MT, Zani S. (1998). New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (nifH) genes. Appl Environ Microbiol 64: 3444-3450.
66. Zehr JP, Paerl HW. (1998). Nitrogen fixation in the marine environment: genetic potential and nitrogenase expression. in Cooksey KE (ed). Molecular approaches to the st udy of the ocean. Chapman & Hall: London, pp 285-301.
67. Zehr JP, Turner PJ. (2001). Nitrogen fixation: nitrogenase genes and gene expression. Methods in Microbiol 30: 271-286.
68. Zehr JP, Waterbury JB, Turner PJ, Montoya JP, Omoregie E, Steward GF et al. (2001). Unicellular Cyanobacteria fix N-2 in the subtropical North Pacific Ocean. Nature 412: 635-638.
69. Zhang J-Z. (2000). Shipboard automatic determination of trace concentrations of nitrite and nitrate in oligotrophic water by gas-segmented continuous flow analysis with a liquid waveguide capillary flow cell. Deep Sea Res I-Oceanogr Res Paper 47: 1157-1171.