Effect of East Asian aerosol enrichment on microbial community composition in the South China Sea

Journal of Plankton Research

Volumn 35, Issue 3, 2013, Pages 485-503

  Guo, Cui ^a   Jing, Hongmei ^a   Kong, Liangliang ^a   Liu, Hongbin ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

Author keywords

abundance and community composition; East Asian aerosol; heterotrophic bacteria; picocyanobacteria; South China Sea

Indexed keywords

ABUNDANCE; AEROSOL; ATMOSPHERIC DEPOSITION; CARBON DIOXIDE; COMMUNITY COMPOSITION; MICROBIAL COMMUNITY; MORTALITY; NUTRIENT ENRICHMENT; OLIGOTROPHIC ENVIRONMENT;

FAR EAST; PACIFIC OCEAN; SOUTH CHINA SEA;

EID: 84877315919     PISSN: 01427873     EISSN: 14643774     Source Type: Journal    
DOI: 10.1093/plankt/fbt002     Document Type: Article

References (76)

1. Aguilar-Islas, A. M., Wu, J., Rember, R. et al. (2010) Dissolution of aerosol-derived iron in seawater: Leach solution chemistry, aerosol type, and colloidal iron fraction. Mar. Chem., 120, 25-33.
2. Allers, E., Gómez-Consarnau, L., Pinhassi, J. et al. (2007) Response of Alteromonadaceae and Rhodobacteriaceae to glucose and phosphorus manipulation in marine mesocosms. Environ. Microbiol., 9, 2417-2429.
3. Beardsley, C., Pernthaler, J., Wosniok, W. et al. (2003) Are readily culturable bacteria in coastal North Sea waters suppressed by selective grazing mortality? Appl. Environ. Microbiol., 69, 2624-2630.
4. Bonnet, S., Guieu, C. C., Chiaverini, J. et al. (2005) Effect of atmospheric nutrients on the autotrophic communities in a low nutrient, low chlorophyll system. Limnol. Oceanogr., 50, 1810-1819.
5. Brand, L., Sunda, W. and Guillard, R. (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. J. Exp. Mar. Biol. Ecol., 96, 225-250.
6. Buchan, A., Gonzalez, J. M. and Moran, M. A. (2005) Overview of the marine Roseobacter lineage. Appl. Environ. Microbiol., 71, 5665-5677.
7. Calbet, A. and Landry, M. R. (2004) Phytoplankton growth, micro-zooplankton grazing, and carbon cycling in marine systems. Limnol. Oceanogr., 49, 51-57.
8. Campbell, L., Nolla, H. A. and Vaulot, D. (1994) The importance of Prochlorococcus to community structure in the central North Pacific Ocean. Limnol. Oceanogr., 39, 954-961.
9. Chen, B., Liu, H., Landry, M. R. et al. (2009) Close coupling between phytoplankton growth and microzooplankton grazing in the western South China Sea. Limnol. Oceanogr., 54, 1084-1097.
10. Chen, Y.-L. L., Chen, H.-Y., Karl, D. M. et al. (2004) Nitrogen modulates phytoplankton growth in spring in the South China Sea. Cont. Shelf Res., 24, 527-541.
11. Chung, C.-C., Chang, J., Gong, G.-C. et al. (2010) Effects of Asian dust storms on Synechococcus populations in the subtropical Kuroshio current. Mar. Biotechnol., 13, 751-763.
12. Cohen, D. D., Garton, D., Stelcer, E. et al. (2004) Multielemental analysis and characterization of fine aerosols at several key ACE-Asia sites. J. Geophys. Res., 109, D19S12.
13. Duce, R. A., Liss, P. S., Merrill, J. T. et al. (1991) The atmospheric input of trace species to the world ocean. Global Biogeochem. Cycles, 5, 193-259.
14. Gao, Y., Aromoto, R., Duce, R. A. et al. (1997) Temporal and spatial distribution of dust and its deposition to the China Sea. Tellus, 49B, 172-189.
15. Gasol, J. M. and del Giorgio, P. A. (2000) Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Marina., 64, 197-224.
16. Gasol, J. M., Giorgio, P. a. D., Massana, R. et al. (1995) Active versus inactive bacteria: size-dependence in a coastal marine plankton community. Mar. Ecol. Prog. Ser., 128, 91-97.
17. Gong, G.-C., Chang, J. and 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.
18. González, J. M., Kiene, R. P. and Moran, M. A. (1999) Transformation of sulfur compounds by an abundant lineage of marine bacteria in the a-subclass of the class Proteobacteria. Appl. Environ. Microbiol., 65, 3810-3819.
19. González, J. M. and Moran, M. A. (1997) Numerical dominance of a group of marine bacteria in the a-subclass of the class Proteobacteria in coastal seawater. Appl. Environ. Microbiol., 64, 4237-4242.
20. González, J. M., Simó, R., Massana, R. et al. (2000) Bacterial community structure associated with a dimethylsulfoniopropionate- producing North Atlantic algal bloom. Appl. Environ. Microbiol., 66, 4237-4246.
21. Grossart, H.-P., Czub, G. and Simon, M. (2006) Algae-bacteria interactions and their effects on aggregation and organic matter flux in the sea. Environ. Microbiol., 8, 1074-1084.
22. Guo, C., Yu, J., Ho, T. Y. et al. (2012) Dynamics of phytoplankton community structure in the South China Sea in response to the East Asian aerosol input. Biogeosciences, 9, 1519-1536.
23. Hahn, M. W. and Höfle, M. G. (2001) Grazing of protozoa and its e¡ect on populations of aquatic bacteria. FEMS Microb. Ecol., 35, 113-121.
24. Hannen, E. J. V., Veninga, M., Bloem, J. et al. (1999) Genetic changes in the bacterial community structure associated with protistan grazers. Arch. Hydrobiol., 145, 25-38.
25. Herut, B., Zohary, T., Krom, M. D. et al. (2005) Response of East Mediterranean surface water to Saharan dust: on-board microcosm experiment and field observations. Deep-Sea Res. II, 52, 3024-3040.
26. Hill, P. G., Zubkov, M. V. and Purdie, D. A. (2010) Differential responses of Prochlorococcus and SAR11-dominated bacterioplankton groups to atmospheric dust inputs in the tropical Northeast Atlantic Ocean. FEMS Microbiol. Lett., 306, 82-89.
27. Hsu, S.-C., Wong, G. T. F., Gong, G.-C. et al. (2010) Sources, solubility, and dry deposition of aerosol trace elements over the East China Sea. Mar. Chem., 120, 116-127.
28. Jasti, S., Sieracki, M. E., Poulton, N. J. et al. (2005) Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Appl. Environ. Microbiol., 71, 3483-3494.
29. Jing, H. and Liu, H. (2012) Phylogenetic composition of Prochlorococcus and Synechococcus in cold eddies of the South China Sea. Aquat. Microb. Ecol., 65, 207-219.
30. Jochem, F. J., Lavrentyev, P. J. and First, M. R. (2004) Growth and grazing rates of bacteria groups with different apparent DNA content in the Gulf of Mexico. Mar. Biol., 145, 1213-1225.
31. Johnson, Z. I., Zinser, E. R., Coe, A. et al. (2006) Niche partitioning among Prochlorococcus ecotypes along ocean-scale environmental gradients. Science, 311, 1737-1740.
32. Kent, A. D., Yannarell, A. C., Rusak, J. A. et al. (2007) Synchrony in aquatic microbial community dynamics. ISME J., 1, 38-47.
33. Knap, A., Michael, A., Close, A. et al. (eds) 1996, Protocols for the Joint Global Ocean Flux Study (JGOFS) core measurements. JGOFS Report Nr. 19, Vi170 pp (reprint of the IOC Manuals and Guides No. 29, UNESCO 1994), pp. 43-110.
34. Kong, L., Jing, H., Kataoka, T. et al. (2011) Phylogenetic diversity and spatio-temporal-distribution of nitrogenase genes (nifH) in the northern South China Sea. Aquat. Microb. Ecol., 65, 15-27.
35. Laghdass, M., Blain, S., Besseling, M. et al. (2011) Effects of Saharan dust on the microbial community during a large in situ mesocosm experiment in the NW Mediterranean Sea. Aquat. Microb. Ecol., 62, 201-213.
36. Landry, M. R., Constantinou, J., Latasa, M. et al. (2000) Biological response to iron fertilization in the eastern equatorial Pacific (IronEx II).III. Dynamics of phytoplankton growth and microzoo-plankton grazing. Mar. Ecol. Prog. Ser., 201, 73-83.
37. Lebaron, P., Servais, P., Baudoux, A.-C. et al. (2002) Variations of bacterial-specific activity with cell size and nucleic acid content assessed by flow cytometry. Aquat. Microb. Ecol., 28, 131-140.
38. Lekunberri, I., Lefort, T., Romero, E. et al. (2010) Effects of a dust deposition event on coastal marine microbial abundance and activity, bacterial community structure and ecosystem function. J. Plankton Res., 32, 381-396.
39. Li, W. K. W. (1994) Primary production of prochlorophytes, cyanobac-teria, and eucaryotic ultraphytoplankton: measurements from flow cytometric sorting. Limnol. Oceanogr., 39, 169-175.
40. Lin, I.-I., Chen, J.-P., Wong, G. T. F. et al. (2007) Aerosol input to the South China Sea: results from the MODerate resolution imaging spectro-radiometer, the quick scatterometer, and the measurements of pollution in the troposphere sensor. Deep-Sea Res II, 54, 1589-1601.
41. Liu, H., Chang, J., Tseng, C.-M. et al. (2007) Seasonal variability of picoplankton in the Northern South China Sea at the SEATS station. Deep-Sea Res II, 54, 1602-1616.
42. Liu, H., Nolla, H. A. and Campbell, L. (1997) Prochlorococcus growth rate and contribution to primary production in the equatorial and subtropical North Pacific Ocean. Aquat. Microb. Ecol., 12, 39-47.
43. Longnecker, K., Sherr, B. F. and Sherr, E. B. (2005) Activity and phylogenetic diversity of bacterial cells with high and low nucleic acid content and electron transport system activity in an upwelling ecosystem. Appl. Environ. Microbiol., 71, 7737-7749.
44. Mann, E. L., Ahlgren, N., Moffett, J. W. et al. (2002) Copper toxicity and cyanobacteria ecology in the Sargasso Sea. Limnol. Oceanogr., 47, 976-988.
45. Marañón, E., Fernández, A., Mouriño-Carballido, B. et al. (2010) Degree of oligotrophy controls the response of microbial plankton to Saharan dust. Limnol. Oceanogr., 55, 2339-2352.
46. Martin, J. H., Gordon, R. M. and Fitzwater, S. E. (1991) The case for iron, Limnol. Oceanogr., 36, 1793-1802.
47. Muyzer, G., Hottenträger, S., Teske, A. et al. (1996) Denaturing gradient gel electrophoresis of PCR amplified 16S rDNA-a new molecular approach to analyze the genetic diversity of mixed microbial communities. In Akkermans, A., Elsas, J. V. and Bruijn, F. D. (eds), Molecular Microbial Ecology Manual 3.4.4. Kluwer Academic Publishing, Dordrecht.
48. Olson, R., Zettler, E. and Durand, M. (1993) Phytoplankton analysis using flow cytometry. In Kemp, P., Sherr, B., Sherr, E. and Cole, J. (eds), Handbook of Methods in Aquatic Microbial Ecology. Lewis.Lewis Publishers, Boca Raton, pp. 175-186.
49. Ortega-Retuerta, E., Reche, I., Pulido-Villena, E. et al. (2008) Exploring the relationship between active bacterioplankton and phytoplankton in the Southern Ocean. Aquat. Microb. Ecol., 52, 99-106.
50. Paerl, H. W. (1997) Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as "new" nitrogen and other nutrient sources. Limnol. Oceanogr., 42, 1154-1165.
51. Paytan, A., Mackey, K. R. M., Chen, Y. et al. (2009) From the Cover: toxicity of atmospheric aerosols on marine phytoplankton. Proc. Natl Acad. Sci. USA, 106, 4601-4605.
52. Pinhassi, J. and Berman, T. (2003) Differential growth response of colony-forming a-and g-proteobacteria in dilution culture and nutrient addition experiments from Lake Kinneret (Israel), the Eastern Mediterranean Sea, and the Gulf of Eilat. Appl. Environ. Microbiol., 69, 199-211.
53. Pinhassi, J., Sala, M. M., Havskum, H. et al. (2004) Changes in bacter-ioplankton composition under different phytoplankton regimens. Appl. Environ. Microbiol., 70, 6753-6766.
54. Pukall, R., Paëuker, O., Buntefum, D. et al. (1999) High sequence diversity of Alteromonas macleodii-related cloned and cellular 16S rDNAs from a Mediterranean seawater mesocosm experiment. FEMS Microb. Ecol., 28, 335-344.
55. Pulido-Villena, E., Wagener, T. and Guieu, C. (2008) Bacterial response to dust pulses in the western Mediterranean: Implications for carbon cycling in the oligotrophic ocean. Global Biogeochem. Cycles, 22, GB1020.
56. Quigg, A., Finkel, Z. V., Irwin, A. J. et al. (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature, 425, 291-294.
57. Reche, I., Ortega-Retuerta, E., Romera, O. et al. (2009) Effect of Saharan dust inputs on bacterial activity and community composition in Mediterranean lakes and reservoirs. Limnol. Oceanogr., 54, 869-879.
58. Rocap, G., Larimer, F. W., Lamerdin, J. et al. (2003) Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424, 1042-1047.
59. Rooney-Varga, J. N., Giewat, M. W., Savin, M. C. et al. (2005) Links between phytoplankton and bacterial community dynamics in a coastal marine environment. Microb. Ecol., 49, 163-175.
60. Schäfer, H., Abbas, B., Witte, H. et al. (2002) Genetic diversity of 'satellite' bacteria present in cultures of marine diatoms. FEMS Microb. Ecol., 45, 25-35.
61. Schäfer, H., Bernard, L., Courties, C. et al. (2001) Microbial community dynamics in Mediterranean nutrient-enriched seawater meso-cosms: changes in the genetic diversity of bacterial populations. FEMS Microb. Ecol., 34, 243-253.
62. Scharek, R. and Latasa, M. (2001) Growth, grazing and carbon flux of high and low nucleic acid bacteria differ in surface and deep chlorophyll maximum layers in the NW Mediterranean Sea. Aquat. Microb. Ecol., 46, 153-167.
63. Schloss, P. and Handelsman, J. (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl. Environ. Microbiol., 71, 1501-1506.
64. Sherr, E. B. and Sherr, B. F. (2002) Significance of predation by pro-tists in aquatic microbial food webs. Mar. Biol., 81, 293-308.
65. Tamura, K., Dudley, J., Nei, M. et al. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol., 24, 1596-1599.
66. Uematsu, M., Yoshikawa, A., Muraki, H. et al. (2002) Transport of mineral and anthropogenic aerosols during a Kosa event over East Asia. J. Geophys. Res., 10, 4059.
67. Wong, G. T. F., Chung, S.-W., Shiah, F.-K. et al. (2002) Nitrate anomaly in the upper nutricline in the northern South China Sea-evidence for nitrogen fixation. Geophys. Res. Lett., 29, 2097.
68. Worden, A. Z. and Binder, B. J. (2003) Application of dilution experiments for measuring growth and mortality rates among Prochlorococcus and Synechococcus populations in oligotrophic environments. Aquat. Microb. Ecol., 30, 159-174.
69. Wu, J., Chung, S.-W., Wen, L.-S. et al. (2003) Dissolved inorganic phosphorus, dissolved iron, and Trichodesmium in the oligotrophic South China Sea. Global Biogeochem. Cycles, 17, 1008-1020.
70. Yuan, X., He, L., Yin, K. et al. (2011) Bacterial distribution and nutrient limitation in relation to different water masses in the coastal and northwestern South China Sea in late summer. Cont. Shelf Res., 31, 1214-1223.
71. Zhang, X., Zhuang, G., Guo, J. et al. (2007) Characterization of aerosol over the Northern South China Sea during two cruises in 2003. Atmos. Environ., 41, 7821-7836.
72. Zubkov, M., Ph, B. and Topping, J. (2007) Flow cytometric enumeration of DNA-stained oceanic planktonic protists. J. Plankton Res., 29, 79-86.
73. Zubkov, M. V., Fuchs, B. M., Burkill, P. H. et al. (2001) Comparison of cellular and biomass specific activities of dominant bacterioplankton groups in stratified waters of the Celtic Sea. Appl. Environ. Microbiol., 67, 5210-5218.
74. Zubkov, M. V., Sleigh, M., Burkill, P. H. et al. (2000) Bacterial growth and grazing loss in contrasting areas of North and South Atlantic. J. Plankton Res., 22, 685-711.
75. Zweifel, U. and Hagström, A. (1995) Total counts of marine bacteria include a large fraction of non-nucleoid-containing bacteria (Ghosts). Appl. Environ. Microbiol., 61, 2180-2185.
76. Zwirglmaier, K., Jardillier, L., Ostrowski, M. et al. (2008) Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ. Microbiol., 10, 147-161.