Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export

ISME Journal

Volumn 7, Issue 12, 2013, Pages 2340-2348

  Bar Zeev, Edo ^a,c   Avishay, Itamar ^a   Bidle, Kay D ^b   Berman Frank, Ilana ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b RUTGERS UNIVERSITY   (United States)

^c Yale University   (United States)

Author keywords

bloom; carbon and nitrogen export flux; programmed cell death; Trichodesmium

Indexed keywords

CARBON; NITROGEN; SEA WATER;

APOPTOSIS; BIOLOGICAL PUMP; CARBON FLUX; CYANOBACTERIUM; MARINE ECOSYSTEM; NITROGEN CYCLE; WATER COLUMN;

ARTICLE; CYANOBACTERIUM; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHYSIOLOGY; SEA; TIME;

CARBON; CYANOBACTERIA; LIGHT; NITROGEN; NITROGEN FIXATION; OCEANS AND SEAS; SEAWATER; TIME FACTORS;

TRICHODESMIUM;

EID: 84888203866     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2013.121     Document Type: Article

References (47)

1. Azam F, Malfatti F. (2007). Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782-791 (Pubitemid 47423766)
2. Arístegui J, Gasol JM, Duarte CM, Herndl GJ. (2009). Microbial oceanography of the dark ocean?s pelagic realm. Limnol Oceanogr 54: 1501-1529
3. Banks J. (1770). the Endeavour Journal of Sir Joseph Banks. Captain James Cook daily Journal, Vol. 1, http://southseas.nla.gov.au/journals/cook/17700828
4. Bar-Zeev E, Berman T, Rahav E, Dishon G, Herut B, Kress N et al. (2011). Transparent exopolymer particle (TEP) dynamics in the eastern Mediterranean Sea. Mar Ecol Prog Ser 431: 107-118
5. Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ. (2012). Trichodesmium-a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol Rev 37: 286-302
6. Berman-Frank I, Bidle KD, Haramaty L, Falkowski PG. (2004). the demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol Oceanogr 49: 997-1005 (Pubitemid 39040337)
7. Berman-Frank I, Rosenberg G, Levitan O, Haramaty L, Mari X. (2007). Coupling between autocatalytic cell death and transparent exopolymeric particle production in the marine cyanobacterium Trichodesmium. Environ Microbiol 9: 1415-1422 (Pubitemid 46763520)
8. Bidle KD, Falkowski PG. (2004). Cell death in planktonic photosynthetic microorganisms. Nat Rev Microbiol 2: 643-655 (Pubitemid 39200047)
9. Bidle KD, Bender SJ. (2008). Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom, thalassiosira pseudonana. Eukaryot Cell 7: 223-236 (Pubitemid 351959689)
10. Boyd PW, Trull TW. (2007). Understanding the export of biogenic particles in oceanic waters: is there consensus? Prog Oceanogr 72: 276-312 (Pubitemid 46367203)
11. Buesseler KO, Lamborg CH, Boyd PW, Lam PJ, Trull TW, Bidigare RR et al. (2007). the Ocean?s twilight zone. Science 316: 567-570
12. Burd BA, Jackson AG. (2009). Particle aggregation. Annu Rev Mar Sci 1: 65-90
13. Capone DG, Subramaniam A, Montoya JP, Voss M, Humborg C, Johansen AM et al. (1998). An extensive bloom of the N2-fixing cyanobacterium Trichodesmium erythraeum in the central Arabian Sea. Mar Ecol Prog Ser 172: 281-292 (Pubitemid 28510192)
14. Castruita M, Elmegreen LA, Shaked Y, Stiefel EI, Morel FMM. (2007). Comparison of the kinetics of iron release from a marine (Trichodesmium erythraeum) Dps protein and mammalian ferritin in the presence and absence of ligands. J Inorg Biochem 101: 1686-1691 (Pubitemid 47576226)
15. Chappell PD, Webb E. (2010). A molecular assessment of the iron stress response in the two phylogenetic clades of Trichodesmium. Environ Microbiol 12: 13-27
16. Chen YB, Zehr JP, Mellon M. (1996). Growth and nitrogen fixation of the diazotrophic filamentous nonheterocystous cyanobacterium Trichodesmium sp IMS 101 in defined media: evidence for a circadian rhythm. J Phycol 32: 916-923 (Pubitemid 27047802)
17. Cho BC, Azam F. (1988). Major role of bacteria in biogeochemical fluxes in the ocean?s interior. Nature 332: 441-443
18. Dandekar AA, Chugani S, Greenberg EP. (2012). Bacterial quorum sensing and metabolic incentives to cooperate. Science 338: 264-266
19. Darwin CR. (1909). the Voyage of the Beagle Chapter I. Collier PF & Son: New York, NY, USA, p 24
20. De La Rocha CL, Passow U. (2007). Factors influencing the sinking of POC and the efficiency of the biological carbon pump. Deep Sea Res 54: 639-658 (Pubitemid 46783466)
21. Engel A, Passow U. (2001). Carbon and nitrogen content of transparent exopolymer particles (TEP) in relation to their Alcian Blue adsorption. Mar Ecol Prog Ser 219: 1-10 (Pubitemid 32956333)
22. Hmelo LR, Van Mooy BAS, Mincer TJ. (2012). Characterization of bacterial epibionts on the cyanobacterium Trichodesmium. Aquatic Microbial Ecol 67: 1-14
23. Hewson I, Govil S, Capone DG, Carpenter EJ, Fuhrman J. (2004). Evidence of Trichodesmium viral lysis and potential significance for biogeochemical cycling in the oligotrophic ocean. Aquatic Microbial Ecol 36: 1-8 (Pubitemid 39104231)
24. Hewson I, Poretsky RS, Dyhrman ST, Zielinski B, White AE, Tripp HJ et al. (2009b).Microbial community gene expression within colonies of the diazotroph, Trichodesmium, from the Southwest Pacific Ocean. ISME J 3: 1286-1300
25. Karl DM, Michaels A, Bergman B, Capone DG, Carpenter E, Letelier R et al. (2002). Dinitrogen fixation in the world?s oceans. Biogeochemistry 57: 47-98
26. Karl DM, Church MJ, Dore JE, Letelier RM, Mahaffeyd C. (2012). Predictable and efficient carbon sequestration in the North Pacific Ocean supported by symbiotic nitrogen fixation. Proc Natl Acad Sci USA 109: 1842-1849
27. Kerbrat S, Amzil Z, Pawlowiez R, Golubic S, Sibat M, Darius HTet al. (2011). First evidence of Palytoxin and 42-Hydroxy-palytoxin in the marine cyanobacterium Trichodesmium. Mar Drugs 9: 543-560
28. Lugomela C, Lyimo TJ, Bryceson I, Semesi AK, Bergman B. (2002). Trichodesmium in coastal waters of Tanzania: diversity, seasonality, nitrogen and carbon fixation. Hydrobiologia 477: 1-13 (Pubitemid 35301848)
29. Luo Y-W, Doney SC, Anderson LA, Benavides M, Berman-Frank I, Bode A et al. (2012). Database of diazotrophs in global ocean: abundance, biomass and nitrogen fixation rates. Earth Syst Sci Data 4: 47-73
30. McDonnell AMP, Buesseler OK. (2010). Variability in the average sinking velocity of marine particles. Limnol Oceanogr 55: 2085-2096
31. Mulholland MR. (2007). the fate of nitrogen fixed by diazotrophs in the ocean. Biogeosciences 4: 37-51 (Pubitemid 46103379)
32. O?Neil JM. (1998). the colonial cyanobacterium Trichodesmium as a physical and nutritional substrate for the harpacticoid copepod Macrosetella gracilis. J Plankton Res 20: 43-59
33. Passow U, Alldredge A. (1995). A dye-binding assay for the spectrophotometric measurement of transparent exopolymer particles (TEP). Limnol Oceanogr 40: 1326-1335 (Pubitemid 3016462)
34. Passow U. (2002). Transparent exopolymer particles (TEP) in aquatic environments. Prog Oceanogr 55: 287-333 (Pubitemid 35464708)
35. Pfaffl MW. (2001). A new mathematical model for relativequantification in real-time RT-PCR. Nucleic Acids Res 29: E45
36. Rodier M, Le Borgne R. (2010). Population and trophic dynamics of Trichodesmium thiebautii in the SE lagoon of New Caledonia. Comparison with T. erythraeum in the SW lagoon. Mar Pollut Bull 61: 349-359
37. Rodier M, Le Borgne R. (2008). Population dynamics and environmental conditions affecting Trichodesmium spp. (filamentous cyanobacteria) blooms in the south-west lagoon of New Caledonia. J Exp Mar Biol Ecol 358: 20-32
38. Schneider B, Schlitzer R, Fischer G, Nöthig EM. (2003). Depth-dependent elemental compositions of particulate organic matter (POM) in the ocean. Global Biogeochem Cycles 17: 32
39. Smith DC, Simon M, Alldrege AL, Azam F. (1992). Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359: 139-142 (Pubitemid 23374905)
40. Subramaniam A, Carpenter EJ, Falkowski PG. (1999). Bio-optical properties of the marine diazotrophic cyanobacteria Trichodesmium spp a reflectance model for remote-sensing. Limnol Oceanogr 44: 618-627 (Pubitemid 29233654)
41. Tandeau de Marsac N, Houmard J. (1988). Complementary chromatic adaptation: physiological conditions and action spectra. Methods Enzymol 167: 318-328
42. Vardi A, Berman-Frank I, Rozenberg T, Hadas O, Kaplan A, Levine A. (1999). Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress. Curr Biol 9: 1061-1064 (Pubitemid 29456179)
43. Verdugo P, Santschi HP. (2010). Polymer dynamics of DOC networks and gel formation in seawater. Deep Sea Res 57: 1486-1493
44. Verity PG, Robertson CY, Tronzo CR, Andrews MG, Nelson JR, Sieracki ME. (1992). Relationships between cell volume and the carbon and nitrogen content of marine photosynthetic nanoplankton. Limnol Oceanogr 37: 1434-1446
45. Villareal TA, Carpenter EJ. (2003). Buoyancy regulation and the potential for vertical migration in the oceanic cyanobacterium Trichodesmium. Microbial Ecol 45: 1-10 (Pubitemid 36933297)
46. Westberry TK, Siegel DA. (2006). Spatial and temporal distribution of Trichodesmium blooms in the world?s oceans. Global Biogeochem Cycles 20: GB4016
47. Yamada N, Fukuda H, Ogawa H, Saito H, Suzumura M. (2012). Heterotrophic bacterial production and extracellular enzymatic activity in sinking particulate matter in the western North Pacific Ocean. Front Microbiol 3: 379.