A Role for Programmed Cell Death in the Microbial Loop

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Orellana, Mónica V ^a,b   Pang, Wyming L ^a,c   Durand, Pierre M ^d,e   Whitehead, Kenia ^a,f   Baliga, Nitin S ^a,b  

^a INSTITUTE FOR SYSTEMS BIOLOGY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c GENOMATICA INC   (United States)

^d UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^e University of Arizona   (United States)

^f Integral Consulting Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON 14; GLYCEROL;

ALGAL GROWTH; APOPTOSIS; ARTICLE; BIOCHEMISTRY; CARBON MINERALIZATION; DUNALLIELA SALINA; FLOW CYTOMETRY; GREEN ALGA; GROWTH RATE; HALOBACTERIUM SALINARUM; HETEROTROPH; IN VITRO STUDY; ISOTOPE TRACING; NONHUMAN; NUCLEOTIDE SEQUENCE; ORGANIC NUTRIENT; POPULATION DYNAMICS; POPULATION GROWTH; TRANSCRIPTOMICS;

APOPTOSIS; CARBON RADIOISOTOPES; CHLOROPHYTA; ECOSYSTEM; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GLYCEROL; HALOBACTERIUM SALINARUM; LAKES; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; POPULATION DYNAMICS; SALINITY; UTAH;

EID: 84877310919     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062595     Document Type: Article

References (102)

1. Azam F, (1998) Oceanography: Microbial control of oceanic carbon flux: the plot thickens. Science 280: 694-696.
2. Azam F, Malfatti F, (2007) Microbial structuring of marine ecosystems. Nat Rev Microbiol 5: 782-791.
3. Pomeroy LR, (1974) Oceans food web, a changing paradigm. Bioscience 24: 499-504.
4. Azam F, (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10: 257-263.
5. Aluwihare LI, Repeta DJ, Chen RF, (1997) A major biopolymeric component to dissolved organic carbon in surface sea water. Nature 387: 166-169.
6. Jiao N, Herndl GJ, Hansell DA, Benner R, Kattner G, et al. (2010) Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nat Rev Micro 8: 593-599.
7. Kaiser K, Benner R, (2008) Major bacterial contribution to the ocean reservoir of detrital organic carbon and nitrogen. Limnol Oceanogr 53: 99-112.
8. McCarthy MD, Hedges JI, Benner R, (1998) Major bacterial contribution to marine dissolved organic nitrogen. Science 281: 231-234.
9. Aluwihare LI, Repeta DJ, Pantoja S, Johnson CG, (2005) Two chemically distinct pools of organic nitrogen accumulate in the ocean. Science 308: 1007-1010.
10. Decho AW, (1990) Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr Mar Biol Annu Rev 28: 73-153.
11. Fuhrman JA, (1999) Marine viruses and their biogeochemical and ecological effects. Nature 399: 541-548.
12. Proctor LM, Fuhrman JA, (1990) Viral mortality of marine bacteria and cyanobacteria. Nature 343: 60-62.
13. Suttle CA, (2007) Marine viruses-major players in the global ecosystem. Nature Rev Microbiol 5: 801-812.
14. Vardi A, Van Mooy BAS, Fredricks HF, Popendorf KJ, Ossolinski JE, et al. (2009) Viral glycosphingolipids induce lytic infection and cell death in marine phytoplankton. Science 326: 861-865.
15. Vardi A, Haramaty L, Van Mooy BAS, Fredricks HF, Kimmance SA, et al. (2012) Host-virus dynamics and subcellular controls of cell fate in a natural coccolithophore population. Proc Nat Acad Sci U S A 109: 19327-19332.
16. Chin W-C, Orellana MV, Quesada I, Verdugo P, (2004) Secretion in unicellular marine phytoplankton: demonstration of regulated exocytosis in Phaeocystis globosa. Plant Cell Physiol 45: 535-542.
17. Nagata T, Kirchman D, (1997) Role of submicron particles and colloids in microbial food webs and biogeochemical cycles within marine environments. Adv Microb Ecol 15: 81-103.
18. Strom SL, Ronald Benner, Ziegler S, Dagg MJ, (1997) Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol Oceangr 42: 1364-1374.
19. Berman-Frank I, Bidle K, Haramaty L, Falkowski P, (2004) The demise of the marine cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway. Limnol Oceanogr 49: 997-1005.
20. Bidle KD, Falkowski PG, (2004) Cell death in planktonic, photosynthetic microorganisms. Nat Rev Micro 2: 643-655.
21. Berges JA, Falkowski P, (1998) Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation. Limnol Oceanogr 43: 129-135.
22. Ben-Amotz A, Polle JEW, Subba Rao DV (2009) The alga Dunaliella: biodiversity, physiology, genomics and biotechnology; Ben-Amotz A, Polle JEW, Subba Rao DV, editors: Science Publishers.
23. Stephens DW, Gillespie DM, (1976) Phytoplankton production in the Great Salt Lake, Utah, and a laboratory study of algal response to enrichment. Limnol Oceanogr 21: 74-87.
24. Bardavid RE, Khristo P, Oren A, (2008) Interrelationships between Dunaliella and halophilic prokaryotes in saltern crystallizer ponds. Extremophiles 12: 5-14.
25. Liska AJ, Shevchenko A, Pick U, Katz A, (2004) Enhanced photosynthesis and redox energy production contribute to salinity tolerance in Dunaliella as revealed by homology-based proteomics. Plant Physiol 136: 2806-2817.
26. Oren A, (1993) Availability, uptake and turnover of glycerol in hypersaline environments. FEMS Microb Ecol 12: 15-23.
27. Bogomolni RA, Spudich JL, (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium. Proc Nat Acadof Sci U S A 79: 6250-6254.
28. Spudich EN, Takahashi T, Spudich JL, (1989) Sensory rhodopsins I and II modulate a methylation/demethylation system in Halobacterium halobium phototaxis. Proc Nat Acad of Sci U S A 86: 7746-7750.
29. Spudich JL, (1993) Color sensing in the Archaea: a eukaryotic-like receptor coupled to a prokaryotic transducer. J Bacteriol 175: 7755-7761.
30. Storch K-F, Rudolph J, Oesterhelt D, (1999) Car: a cytoplasmic sensor responsible for arginine chemotaxis in the archaeon Halobacterium salinarum. EMBO J 18: 1146-1158.
31. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, et al. (2004) Systems level insights into the stress response to UV radiation in the halophilic Archaeon Halobacterium NRC-1. Genome Res 14: 1025-1035.
32. Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J, (2005) Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC-1 to desiccation and gamma irradiation. Extremophiles 9: 219-227.
33. Brooun A, Bell J, Freitas T, Larsen RW, Alam M, (1998) An Archaeal aerotaxis transducer combines subunit I core structures of eukaryotic cytochrome c oxidase and eubacterial methyl-accepting chemotaxis proteins. J Bacteriol 180: 1642-1646.
34. DasSarma S, Arora P, Lin F, Molinari E, Yin LR, (1994) Wild-type gas vesicle formation requires at least ten genes in the gvp gene cluster of Halobacterium halobium plasmid pNRC-100. J Bacteriol 176: 7646-7652.
35. Halladay JT, Jones JG, Lin F, MacDonald AB, DasSarma S, (1993) The rightward gas vesicle operon in Halobacterium plasmid pNRC100: identification of the gvpA and gvpC gene products by use of antibody probes and genetic analysis of the region downstream of gvpC. J Bacteriol 175: 684-692.
36. Kokoeva MV, Oesterhelt D, (2000) BasT, a membrane-bound transducer protein for amino acid detection in Halobacterium salinarum. Mol Microbiol 35: 647-656.
37. Fabrizio P, Battistella L, Vardavas R, Gattazzo C, Liou L-L, et al. (2004) Superoxide is a mediator of an altruistic aging program in Saccharomyces cerevisiae. J Cell Biol 166: 1055-1067.
38. Bidle KD, Bender SJ, (2008) Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom Thalassiosira pseudonana. Eukaryot Cell 223: 223-230.
39. Franklin DJ, Brussaard CPD, Berges JA, (2006) What is the role and nature of programmed cell death in phytoplankton ecology? Eur J Phycol 41: 1-44.
40. Segovia M, Haramaty L, Berges JA, Falkowski PG, (2003) Cell Death in the unicellular Chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132: 99-105.
41. Vardi A, Eisenstadt D, Murik O, Berman-Frank I, Zohary T, et al. (2007) Synchronization of cell death in a dinoflagellate population is mediated by an excreted thiol protease. Environ Microbiol pp. 360-369.
42. Nedelcu AM, Driscoll WW, Durand PM, Herron MD, Rashidi A, (2011) On the paradigm of altruistic suicide in the unicellular world. Evolution 65: 3-20.
43. Williams GC (1966) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton, N.J.: Princeton University Press.
44. Durand PM, Rashidi A, Michod RE, (2011) How an organism dies affects the fitness of its neighbors. The American Naturalist 177: 224-232.
45. Franklin DJ, Brussaard CPD, Berges JA, (2006) What is the role and nature of programmed cell death in phytoplankton ecology? Eur J Phycol 41: 1-44.
46. González MA, Coleman AW, Gómez PI, Montoya R, (2001) Phylogenetic relationship among various strains of Dunaliella (Chorophyceae) based on nuclear ITS rDNA sequences. J Phycol 37: 604-611.
47. Ng WV, Kennedy SP, Mahairas GG, Berquist B, Pan M, et al. (2000) Genome sequence of Halobacterium species NRC-1. Proc Natl Acad Sci U S A 97: 12176-12181.
48. Sverdrup Hu, Johnson M, Fleming R (1957) The Oceans: Prentice-Hall, Inc.
49. Chanley MH, Smith WL (1975) Culture of Marine Invertebrate Animals: Proceedings-1st Conference on Culture of Marine Invertebrate Animals Greenport: Springer.
50. Dassarma S, Fleischmann EM (1995) Archaea a Laboratory Manual: Halophiles: Cold Spring Harbor Laboratory Press.
51. Breckenridge LJ, Almers W, (1987) Final steps in exocytosis observed in a cell with giant secretory granules. Nature 84: 1945-1949.
52. Pralong WF, Bartley C, Wollheim CB, (1990) Single islet beta-cell stimulation by nutrients: relationship between pyridine nucleotides, cytosolic Ca2+ and secretion. EMBO J 9: 53-60.
53. Marie D, Partensky F, Jacquet S, Vaulot D, (1997) Enumeration and cell cycle analysis of natural populations of marine picoplankton by flow cytometry using the nucleic acid stain SYBR Green I. Appl Environ Microbiol 63: 186-186.
54. Jiménez C, Capasso JM, Edelstein CL, Rivard CJ, Lucia S, et al. (2009) Different ways to die: cell death modes of the unicellular chlorophyte Dunaliella viridis exposed to various environmental stresses are mediated by the caspase-like activity DEVDase. J Exp Bot 60: 815-828.
55. Moharikar S, D'Souza JS, Kulkarni AB, Rao BJ, (2006) Apoptotic-like cell death pathway is induced in unicellular chlorophyte Chlamydomonas reinhardtii (Chlorophyceae) cells following UV irradiation detection and funtional analysis. J Phycol 42: 423-433.
56. Engelbrecht D, Durand PM, Coetzer TL, (2012) On programmed cell death in Plasmodium falciparum: Status quo. J Trop Med 2012: 646534-646534.
57. Iverson RL, Bittaker HF, Myers VB, (1976) Loss of radiocarbon in direct use of Aquasol for liquid scintillation counting of solutions containing 14C-NaHCO3. Limnol Oceanogr 21: 756-758.
58. Strickland JDH, Parsons TR (1972) A practical handbook of seawater analysis. Ottawa Fisheries Research Board of Canada.
59. Kaur A, Pan M, Meislin M, Facciotti MT, El-Gewely R, et al. (2006) A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res16: 841-854.
60. Whitehead K, Pan M, Masumura K-i, Bonneau R, Baliga NS, (2009) Diurnally entrained anticipatory behavior in Archaea. PLoS ONE 4.
61. Bonneau R, Facciotti MT, Reiss DJ, Schmid AK, Pan M, et al. (2007) A predictive model for transcriptional control of physiology in a free living cell. Cell 131: 1354-1365.
62. Ideker T, Thorsson V, Siegel AF, Hood LE, (2004) Testing for differentially-expressed genes by maximum-likelihood analysis of microarray data. J Comput Biol 7: 805-817.
63. Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. 191 p. PICES Special Publication.
64. Zhang H, Byrne RH, (1996) Spectrophotometric pH measurements of surface seawater at in-situ conditions: absorbance and protonation behavior of thymol blue. Mar Chem 52: 17-25.
65. Droop MR, (1973) Some thoughts on nutrient limitation in algae. J of Phycol 9: 264-272.
66. Ben-Amotz A, Avron M, (1973) The role of glycerol in the osmotic regulation of the halophilic alga Dunaliella parva. Plant Physiol 51: 875-878.
67. Orellana MV, Matrai PA, Janer M, Rauschenberg C, (2010) DMSP storage in Phaeocystis secretory vesicles. J Phycol 47: 112-117.
68. Rao SDV (2009) Cultivation, growth media, division rates and applications of Dunaliella species.; Ben-Amotz AJEWPaDVSR, editor.India: Science Pubublishers. 555 p.
69. Mary I, Garczarek L, Tarran GA, Kolowrat C, Terry MJ, et al. (2008) Diel rhythmicity in amino acid uptake by Prochlorococcus. Environ Microbiol 10: 1927-2190.
70. Tafreshi A, Shariati M, (2006) Pilot culture of three strains of Dunaliella salina for β-carotene production in open ponds in the central region of Iran. World J Microbiol Biotechnol 22: 1003-1006.
71. Fernandez JM, Villalón M, Verdugo P, (1991) Reversible condensation of mast cell secretory products in vitro. Biophys J 59: 1022-1027.
72. Bonneau R, Baliga NS, Deutsch EW, Shannon P, Hood L, (2004) Comprehensive de novo structure prediction in a systems-biology context for the archaea Halobacterium sp. NRC-1. Genome Biology 5: R52.
73. Van PT, Schmid AK, King NL, Kaur A, Pan M, et al. (2008) Halobacterium salinarum NRC-1 Peptide Atlas: toward strategies for targeted proteomics and improved proteome coverage. J Proteome Res 7: 3755-3764.
74. Falkowski PG, Raven JA (2007) Aquatic Photosynthesis.: Princeton University Press.
75. Muller JA, DasSarma S, (2005) Genomic Analysis of anaerobic respiration in the archaeon Halobacterium sp. Strain NRC-1: Dimethyl sulfoxide and trimethylamine N-Oxide as terminal electron acceptors. J Bacteriol 187: 1659-1667.
76. Kirchman DL (2008) Microbial Ecology of the Oceans. Hoboken, New Jersey: John Wiley & Sons, Inc., Publication. 593 p.
77. Bidle KD, Azam F, (1999) Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397: 508-512.
78. Blackburn N, Fenchel T, Mitchell J, (1998) Microscale nutrient patches in planktonic habitats shown by chemotactic bacteria. Science 282: 2254-2256.
79. Leigh Jr EG, (2010) The evolution of mutualism. J Evol Biol23: 2507-2528.
80. Lewis J, Kennaway G, Franca S, Alverca E, (2001) Bacterium-dinoflagellate interactions: investigative microscopy of Alexandrium spp. (Gonyaulacales, Dinophyceae). Phycologia 40: 280-285.
81. Azam F, Long RA, (2001) Oceanography-sea snow microcosms. Nature 414: 495-498.
82. Verdugo P, (2012) Marine microgels. Ann Rev Mar Sci 4: 9.1-9.25.
83. DeLong EF, Pace NR, (2001) Environmental diversity of bacteria and archaea. Syst Biol 50: 470-478.
84. Stephens DW, Gillespie DM, (1976) Phytoplankton production in the Great Salt Lake, Utah, and a laboratory study of algal response to enrichment. Limnol and Oceanog 21: 74-87.
85. Schidlowski M, Matzigkeit U, Krumbein WE, (1984) Superheavy organic carbon from hypersaline microbial mats assimilatory pathway and geochemical implications. Naturwissenschaften 71: 303-308.
86. Riebesell U, Wolf-Gladrow D, Smetacek V, (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361: 249-251.
87. Kaplan A, Reinhold L, (1999) CO2 concentrating mechanisms in photosynthetic microorganisms. Annu Rev Plant Physiol Plant Mol Biol 50: 539-570.
88. Giordano M, Beardall J, Raven JA, (2005) CO2 concentrating mechanisms in algae: mechanism, environmental modulation, and evolution. Annu Rev Plant Biol 56: 99-131.
89. Segovia M, Haramaty L, Berges JA, Falkowski PG, (2003) Cell death in the unicellular chlorophyte Dunaliella tertiolecta: a hypothesis on the evolution of apoptosis in higher plants and metazoans. Plant Physiol 132: 99-105.
90. Bidle KD, Bender SJ, (2008) Iron starvation and culture age activate metacaspases and programmed cell death in the marine diatom Thalassiosira pseudonana. Eukaryot Cell 223: 223-230.
91. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Alnemri ES, et al. (2008) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3-11.
92. Croft MT, Lawrence AD, Raux-Deery E, Warren MJ, Smith AG, (2005) Algae acquire vitamin B12 through a symbiotic relationship with bacteria. Nature 438: 90-93.
93. Droop MR, (2007) Vitamins, phytoplankton and bacteria: symbiosis or scavenging. J Plankton Res 29: 107-113.
94. Lau WWY, Keil RG, Armbrust EV, (2007) Succession and diel transcriptional response of the glycolate-utilizing component of the bacterial community during a spring phytoplankton bloom. Appl Environ Microbiol 73: 2440-2450.
95. Reimann L, Steward GF, Azam F, (2000) Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl Environ Microbiol 66: 578-587.
96. Pace ML, Cole JJ, (1996) Regulation of bacteria by resources and predation tested in whole-lake experiments. Limnol Oceanogr 41: 1448-1460.
97. Rosenzweig ML, (1977) Aspects of biological exploitation. Quarterly Rev Biol 52: 371-380.
98. Payne JW (1980) Transport and utilization of peptides by bacteria. In: Paine JW, editor. Microorganisms and Nitrogen Sources.New York: John Wiley and Sons. pp. 212-256.
99. Liow LH, Van Valen L, Stenseth NC, (2011) Red Queen: from populations to taxa and communities. Trends in ecology & evolution 26: 349-358.
100. Wilkerson CR, (1987) Interoceanic differences in size and nutrition of coral reef sponge populations. Science 236: 16541657.
101. Post FJ, (1981) Microbiology of the Great Salt Lake north arm. Hydrobiologia 81-82: 59-69.
102. Kirchman DL, Malmstrom RR, Cottrell MT, (2005) Control of bacterial growth by temperature and organic matter in the Western Arctic. Deep-Sea Res II 52: 3386-3395.