Effects of Asian Dust Storms on Synechococcus Populations in the Subtropical Kuroshio Current

Marine Biotechnology

Volumn 13, Issue 4, 2011, Pages 751-763

  Chung, Chih Ching ^a   Chang, Jeng ^a   Gong, Gwo Ching ^a   Hsu, Shih Chieh ^b   Chiang, Kuo Ping ^a   Liao, Chia Wen ^a  

^a NATIONAL TAIWAN OCEAN UNIVERSITY   (Taiwan)

^b RESEARCH CENTER FOR ENVIRONMENTAL CHANGES   (Taiwan)

Author keywords

Dust storm; Picophytoplankton; Prochlorococcus; Synechococcus

Indexed keywords

16S RIBOSOMAL RNA; ASIAN DUST STORM; DUST DEPOSITION; DUST STORM; EAST CHINA SEA; IRON DEFICIENCY; KUROSHIO CURRENT; MESSENGER RNAS (MRNA); MRNA LEVEL; NITROGEN DEFICIENCY; NUCLEOTIDE SEQUENCES; NUTRIENT CONCENTRATIONS; NUTRIENT DEFICIENCY; OLIGOTROPHIC REGIONS; PACIFIC OCEAN; PHOSPHORUS DEFICIENCY; PHYLOGENETIC ANALYSIS; PICOPHYTOPLANKTON; PROCHLOROCOCCUS; REVERSE TRANSCRIPTION-POLYMERASE CHAIN REACTION; SHELF BREAK; SYNECHOCOCCUS;

DECELERATION; DUST; NUTRIENTS; OCEAN CURRENTS; PHOSPHORUS; POLYMERASE CHAIN REACTION; RNA;

STORMS;

BACTERIAL PROTEIN; CHLOROPHYLL; CHLOROPHYLL A; DNA BINDING PROTEIN; IDIA PROTEIN, SYNECHOCOCCUS; IRON BINDING PROTEIN; MESSENGER RNA; NTCA PROTEIN, SYNECHOCOCCUS; PERIPLASMIC BINDING PROTEIN; PRIMER DNA; RNA 16S; TRANSCRIPTION FACTOR;

ABUNDANCE; ATMOSPHERIC DEPOSITION; CONCENTRATION (COMPOSITION); CYANOBACTERIUM; DUST STORM; ECOLOGICAL IMPACT; GROWTH RATE; IRON; NITROGEN; NUTRIENT AVAILABILITY; OLIGOTROPHIC ENVIRONMENT; PHOSPHATE; PHYLOGENETICS; PICOPLANKTON; POLYMERASE CHAIN REACTION; POPULATION DECLINE; SHELF BREAK;

ARTICLE; DNA SEQUENCE; DUST; GENETICS; GROWTH, DEVELOPMENT AND AGING; MASS SPECTROMETRY; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PACIFIC OCEAN; PHYTOPLANKTON; POPULATION DYNAMICS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNECHOCOCCUS; WATER FLOW;

BACTERIAL PROTEINS; BASE SEQUENCE; CHLOROPHYLL; DNA PRIMERS; DNA-BINDING PROTEINS; DUST; IRON-BINDING PROTEINS; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; PACIFIC OCEAN; PERIPLASMIC BINDING PROTEINS; PHYTOPLANKTON; POPULATION DYNAMICS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYNECHOCOCCUS; TRANSCRIPTION FACTORS; WATER MOVEMENTS;

KUROSHIO CURRENT; PACIFIC OCEAN;

IDIA; PROCHLOROCOCCUS; SYNECHOCOCCUS;

EID: 79960462680     PISSN: 14362228     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10126-010-9336-5     Document Type: Article

References (71)

1. Bishop JKB, Davis RE, Sherman JT (2002) Robotic observations of dust storm enhancement of carbon biomass in the North Pacific. Science 298: 817-821.
2. Blanchot J, Rodier M (1996) Picophytoplankton abundance and biomass in the western tropical Pacific Ocean during the 1992 El Nino year: results from flow cytometry. Deep Sea Res I 43: 877-895.
3. Boyd PW, Watson AJ, Law CS, Abraham ER, Trull T, Murdoch R, Bakker DCE, Bowie AR, Buesseler KO, Chang H, Charette M, Croot P, Downing K, Frew R, Gall M, Hadfield M, Hall J, Harvey M, Jameson G, LaRoche J, Liddicoat M, Ling R, Maldonado MT, McKay RM, Nodder S, Pickmere S, Pridmore R, Rintoul S, Safi K, Sutton P, Strzepek R, Tanneberger K, Turner S, Waite A, Zeldis J (2000) A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron fertilization. Nature 407: 695-702.
4. Boyd PW, Strzepek R, Takeda S, Jackson G, Wong CS, McKay RM, Law C, Kiyosawa H, Saito H, Sherry N, Johnson K, Gower J, Ramaiah N (2005) The evolution and termination of an iron-induced mesoscale bloom in the northeast subarctic. Pac Limnol Oceanogr 50: 1872-1886.
5. Boyd PW, Jickells T, Law CS, Blain S, Boyle EA, Buesseler KO, Coale KH, Cullen JJ, de Baar HJW, Follows M, Harvey M, Lancelot C, Levasseur M, Owens NPJ, Pollard R, Rivkin RB, Sarmiento J, Schoemann V, Smetacek V, Takeda S, Tsuda A, Turner S, Watson AJ (2007) Mesoscale iron enrichment experiments 1993-2005: synthesis and future directions. Science 315: 612-617.
6. Campbell L, Vaulot D (1993) Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (station ALOHA). Deep Sea Res 40: 2043-2060.
7. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31: 3497-3500.
8. Chiang K-P, Kuo M-C, Chang J, Wang R-H, Gong G-C (2002) Spatial and temporal variation of the Synechococcus population in the East China Sea and its contribution to phytoplankton biomass. Cont Shelf Res 22: 3-13.
9. Chisholm SW, Olson RJ, Zettler ER, Goericke R, Waterbury JB, Welschmeyer NA (1988) A novel free-living prochlorophyte abundant in the oceanic euphotic zone. Nature 334: 340-343.
10. Coale KH, Johnson KS, Fitzwater SE, Gordon RM, Tanner S, Chavez FP, Ferioli L, Sakamoto C, Rogers P, Millero F, Steinberg P, Nightingale P, Cooper D, Cochlan WP, Landry MR, Constantinou J, Rollwagen G, Trasvina A, Kudela R (1996) A massive phytoplankton bloom induced by an ecosystem-scale iron fertilization experiment in the equatorial Pacific Ocean. Nature 383: 495-501.
11. Davey M, Tarran GA, Mills MM, Ridame C, Geider RJ, La Roche J (2008) Nutrient limitation of picophytoplankton photosynthesis and growth in the tropical North Atlantic. Limnol Oceanogr 53: 1722-1733.
12. DeLong EF (2009) The microbial ocean from genomes to biomes. Nature 459: 200-206.
13. DiTullio GR, Laws EA (1991) Impact of an atmospheric-oceanic disturbance on phytoplankton community dynamics in the North Pacific Central Gyre. Deep Sea Res 38: 1305-1329.
14. DuRand MD, Olson RJ, Chisholm SW (2001) Phytoplankton population dynamics at the Bermuda Atlantic time-series station in the Sargasso Sea. Deep Sea Res II 48: 1983-2003.
15. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S, Mackenzie FT, Moore B III, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290: 291-296.
16. Fan TP (2006) The diversity of iron deficiency induced protein A gene (idiA) and nitrogen control gene A (ntcA) in the East China Sea and its application to the design of specific primers. MS dissertation. Institute of Marine Biology. Keelung: National Taiwan Ocean University.
17. Fuller N, Marie D, Partensky F, Vaulot D, Post A, Scanlan D (2003) Clade-specific 16S ribosomal DNA oligonucleotides reveal the predominance of a single marine Synechococcus clade throughout a stratified water column in the Red Sea. Appl Environ Microbiol 69: 2430-2443.
18. Fuller NJ, West NJ, Marie D, Yallop M, Rivlin T, Post AF, Scanlan DJ (2005) Dynamics of community structure and phosphate status of picocyanobacterial populations in the Gulf of Aqaba, Red Sea. Limnol Oceanogr 50: 363-375.
19. Glover HE, Prezelin BB, Campbell L, Campbell M, Garside C (1988) A nitrate-dependent Synechococcus bloom in surface Sargasso Sea water. Nature 331: 161-163.
20. Goericke R, Welschmeyer NA (1993) The marine prochlorophyte Prochlorococcus contributes significantly to phytoplankton biomass and primary production in the Sargasso Sea. Deep Sea Res I 40: 2283-2294.
21. Goldman JC (1993) Potential role of large oceanic diatoms in new primary production. Deep Sea Res I 40: 159-168.
22. Gong G-C, Chen Y-L, Liu K-K (1996) Summertime hydrography and chlorophyll a distribution in the East China Sea in summer: implications of nutrient dynamics. Cont Shelf Res 16: 1561-1590.
23. Gong G-C, Shiah F-K, Liu K-K, Chuang W-S, Chang J (1997) Effect of the Kuroshio intrusion on the chlorophyll distribution in the southern East China Sea during spring 1993. Cont Shelf Res 17: 79-94.
24. Gong G-C, Chang J, Wen Y-H (1999) Estimation of annual primary production in the Kuroshio waters northeast of Taiwan using a photosynthesis-irradiance model. Deep Sea Res I 46: 93-108.
25. Gong G-C, Shiah F-K, Liu K-K, Wen Y-H, Liang M-H (2000) Spatial and temporal variation of chlorophyll a, primary productivity and chemical hydrography in the southern East China Sea. Cont Shelf Res 20: 411-436.
26. Goudie AS, Middleton NJ (2001) Saharan dust storms: nature and consequences. Earth Sci Rev 56: 179-204.
27. Hernández-León S, Almeida C, Bécognée P, Yebra L, Arístegui J (2004) Zooplankton biomass and indices of grazing and metabolism during a late winter bloom in subtropical waters. Mar Biol 145: 1191-1200.
28. Herut B, Zohary T, Krom MD, Mantoura RFC, Pitta P, Psarra S, Rassoulzadegan F, Tanaka T, Thingstad TF (2005) Response of East Mediterranean surface water to Saharan dust: on-board microcosm experiment and field observations. Deep Sea Res II 52: 3024-3040.
29. Hsu S-C, Liu SC, Huang Y-T, Lung S-CC, Tsai F, Tu J-Y, Kao S-J (2008) A criterion for identifying Asian dust events based on Al concentration data collected from northern Taiwan between 2002 and early 2007. J Geophys Res 113: D18306.
30. Hsu S-C, Liu SC, Arimoto R, Liu T-H, Huang Y-T, Tsai F, Lin F-J, Kao S-J (2009) Dust deposition to the East China Sea and its biogeochemical implications. J Geophys Res 114: D15304.
31. Hsu S-C, Wong GTF, Gong G-C, Shiah F-K, Huang Y-T, Kao S-J, Tsai F, Candice Lung S-C, Lin F-J, Lin II, Hung C-C, Tseng C-M (2010) Sources, solubility, and dry deposition of aerosol trace elements over the East China Sea. Mar Chem 120: 116-127.
32. Hung C-C, Gong G-C, Chung W-C, Kuo W-T, Lin F-C (2009) Enhancement of particulate organic carbon export flux induced by atmospheric forcing in the subtropical oligotrophic northwest Pacific Ocean. Mar Chem 113: 19-24.
33. Hung S-H (2009) The expression of pstS in the East China Sea picoplankton community: primer design and field tests. MS dissertation. Institute of Marine Environmental Chemistry and Ecology. Keelung: National Taiwan Ocean University.
34. Jiao N, Yang Y, Koshikawa H, Watanabe M (2002) Influence of hydrographic conditions on picoplankton distribution in the East China Sea. Aquat Microb Ecol 30: 37-48.
35. Jickells TD (1995) Atmospheric inputs of metals and nutrients to the oceans: their magnitude and effects. Mar Chem 48: 199-214.
36. Jickells TD, An ZS, Andersen KK, Baker AR, Bergametti G, Brooks N, Cao JJ, Boyd PW, Duce RA, Hunter KA, Kawahata H, Kubilay N, laRoche J, Liss PS, Mahowald N, Prospero JM, Ridgwell AJ, Tegen I, Torres R (2005) Global iron connections between desert dust, ocean biogeochemistry, and climate. Science 308: 67-71.
37. Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic, New York, pp 21-132.
38. Katano T, Kaneda A, Kanzaki N, Obayashi Y, Morimoto A, Onitsuka G, Yasuda H, Mizutani S, Kon Y, Hata K, Takeoka H, Nakano S-I (2007) Distribution of prokaryotic picophytoplankton from Seto Inland Sea to the Kuroshio region, with special reference to 'Kyucho' events. Aquat Microb Ecol 46: 191-201.
39. Kellogg CA, Griffin DW (2006) Aerobiology and the global transport of desert dust. Trends Ecol Evol 21: 638-644.
40. Lindell D, Post AF (1995) Ultraphytoplankton succession is triggered by deep winter mixing in the Gulf of Aqaba (Eilat), Red Sea. Limnol Oceanogr 40: 1130-1141.
41. Lindell D, Post AF (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.
42. Lindell D, Penno S, Al-Qutob M, David E, Rivlin T, Lazar B, Post AF (2005) Expression of the nitrogen stress response gene ntcA reveals nitrogen-sufficient Synechococcus populations in the oligotrophic northern Red Sea. Limnol Oceanogr 50: 1932-1944.
43. Liu CM, Young CY, Lee YC (2006) Influence of Asian dust storms on air quality in Taiwan. Sci Total Environ 368: 884-897.
44. Liu H, Campbell L, Landry MR (1995) Growth and mortality rates of Prochlorococcus and Synechococcus measured with a selective inhibitor technique. Mar Ecol Prog Ser 116: 277-287.
45. Liu H, Nolla HA, Campbell L (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat Microb Ecol 12: 9-47.
46. Luque I, Flores E, Herrero A (1994) Molecular mechanism for the operation of nitrogen control in cyanobacteria. EMBO J 13: 2862-2869.
47. Mann EL, Ahlgren N, Moffett JW, Chisholm SW (2002) Copper toxicity and cyanobacteria ecology in the Sargasso Sea. Limnol Oceanogr 47: 976-988.
48. Mills 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.
49. Moore LR, Post AF, Rocap G, Chisholm SW (2002) Utilization of different nitrogen sources by the marine cyanobacteria Prochlorococcus and Synechococcus. Limnol Oceanogr 47: 989-996.
50. Moutin T, Thingstad TF, van Wambeke F, Marie D, Slawyk G, Raimbault P, Claustre H (2002) Does competition for nanomolar phosphate supply explain the predominance of the cyanobacterium Synechococcus? Limnol Oceanogr 47: 1562-1567.
51. Neuer S, Torres-Padrón M, Gelado-Caballero M, Rueda M, Hernández-Brito J, Davenport R, Wefer G (2004) Dust deposition pulses to the eastern subtropical North Atlantic gyre: does ocean's biogeochemistry respond? Glob Biogeochem Cycles 18: GB4020.
52. Nitani H (1972) Beginning of the Kuroshio. In: Stommel H, Yoshida K (eds) Kuroshio. University of Washington Press, Seattle, pp 129-163.
53. Pai S-C, Tsau Y-J, Yang T-I (2001) pH and buffering capacity problems involved in the determination of ammonia in saline water using the indophenol blue spectrophotometric method. Anal Chim Acta 434: 209-216.
54. Partensky F, Blanchot J, Vaulot D (1999a) Differential distribution and ecology of Prochlorococcus and Synechococcus in oceanic waters: a review. Bull Inst Océanogr Monaco 19: 457-475.
55. Partensky F, Hess WR, Vaulot D (1999b) Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol Mol Biol Rev 63: 106-127.
56. Paytan A, Mackey KRM, Chen Y, Lima ID, Doney SC, Mahowald N, Labiosa R, Post AF (2009) Toxicity of atmospheric aerosols on marine phytoplankton. Proc Natl Acad Sci USA 106: 4601-4605.
57. Post AF (2005) Nutrient limitation of marine cyanobacteria-molecular ecology in an oligotrophic sea. In: Huisman J, Matthijs HCP, Visser PM (eds) Harmful cyanobacteria. Springer, Netherlands, pp 87-107.
58. Richardson TL, Jackson GA (2007) Small phytoplankton and carbon export from the surface ocean. Science 315: 838-840.
59. Rivers AR, Jakuba RW, Webb EA (2009) Iron stress genes in marine Synechococcus and the development of a flow cytometric iron stress assay. Environ Microbiol 11: 382-396.
60. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, Arellano A, Coleman M, Hauser L, Hess WR, Johnson ZI, Land M, Lindell D, Post AF, Regala W, Shah M, Shaw SL, Steglich C, Sullivan MB, Ting CS, Tolonen A, Webb EA, Zinser ER, Chisholm SW (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424: 1042-1047.
61. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73: 249-299.
62. Smith CJ, Osborn AM (2009) Advantages and limitations of quantitative PCR(Q-PCR)-based approaches in microbial ecology. FEMS Microbiol Ecol 67: 6-20.
63. Ting CS, Rocap G, King J, Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends Microbiol 10: 134-142.
64. Waterbury JB, Watson SW, Guillard RRL, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium. Nature 277: 293-294.
65. Webb EA, Moffett JW, Waterbury JB (2001) Iron stress in open-ocean cyanobacteria (Synechococcus, Trichodesmium, and Crocosphaera spp.): identification of the idiA protein. Appl Environ Microbiol 67: 5444-5452.
66. West NJ, Schonhuber WA, Fuller NJ, Amann RI, Rippka R, Post AF, Scanlan DJ (2001) Closely related Prochlorococcus genotypes show remarkably different depth distributions in two oceanic regions as revealed by in situ hybridization using 16S rRNA-targeted oligonucleotides. Microbiology 147: 1731-1744.
67. Wong GTF, Chao S-Y, Li Y-H, Shiah F-K (2000) The Kuroshio edge exchange process (KEEP) study-an introduction to hypotheses and highlights. Cont Shelf Res 20: 335-347.
68. Yuan W, Zhang J (2006) High correlations between Asian dust events and biological productivity in the western North Pacific. Geophys Res Lett 33: L07603.
69. Zohary T, Herut B, Krom MD, Fauzi C, Mantoura R, Pitta P, Psarra S, Rassoulzadegan F, Stambler N, Tanaka T, Thingstad TF, Woodward EMS (2005) P-limited bacteria but N and P co-limited phytoplankton in the Eastern Mediterranean-a microcosm experiment. Deep Sea Res II 52: 3011-3023.
70. Zwirglmaier K, Heywood JL, Chamberlain K, Woodward EMS, Zubkov MV, Scanlan DJ (2007) Basin-scale distribution patterns of picocyanobacterial lineages in the Atlantic Ocean. Environ Microbiol 9: 1278-1290.
71. Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10: 147-161.