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The Yellow Sea Warm Current flushes the Bohai Sea microbial community in winter

Caixia Wang https://orcid.org/0000-0003-2847-5959 A C D , Yibo Wang A B C , Pengyuan Liu A B C , Lin Wu A , James S. Paterson D , James G. Mitchell D , Andrew T. Revill E and Xiaoke Hu A C F
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Coastal Biology and Bioresource Utilisation, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, 17# Chunhui Road, Laishan District, Yantai 264003, China.

B University of Chinese Academy of Sciences, No.19(A) Yuquan Road, Shijingshan District, Beijing 100049, China.

C Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China.

D School of Biological Sciences, Flinders University, GPO Box 2100, Adelaide, SA 5001, Australia.

E CSIRO Oceans and Atmosphere, GPO Box 1538, Hobart, Tas. 7001, Australia.

F Corresponding author. Email: xkhu@yic.ac.cn

Marine and Freshwater Research 71(12) 1616-1627 https://doi.org/10.1071/MF19399
Submitted: 29 December 2019  Accepted: 15 May 2020   Published: 4 July 2020

Abstract

The effect of the Yellow Sea Warm Current (YSWC) on virio- and bacterioplankton communities in the Bohai Sea is unknown. In this study, the composition and dynamic changes of virio- and bacterioplankton at the entrance of the Bohai Sea were measured to determine the influence of the YSWC on those communities and vice versa. In the Bohai Strait, there were east to west gradients of water chemistry and hydrology. The turbulent mixing between the deep north-western ‘warm’ current, which is 9°C, and the cold, nutrient-rich Bohai Sea water at 7–8°C appears to stimulate the abundance of both viruses and heterotrophic bacteria, with numbers at the junction of ‘warm’ and cold water being almost 10-fold greater than in the low-thermohaline areas, and peaking where the temperature is the highest. The average viral and bacterial abundances in the north-eastern area are much higher than in the south-western area. It proved that the YSWC entered the Bohai Sea with poor biomass and exited with rich biomass, which, in turn, enriches the Yellow Sea microbial loop. Our results showed the dramatic effect of temperature rise and increasing eutrophication on microbial abundance and marine microbial communities.

Additional keywords: bacterioplankton, biomass, eutrophication, flow cytometry, virioplankton.


References

Alonso, M., Jiminez-Gomez, F., Rodriguez, J., and Borrego, J. (2001). Distribution of virus-like particles in an oligotrophic marine environment (Alboran Sea, Western Mediterranean). Microbial Ecology 42, 407–415.
Distribution of virus-like particles in an oligotrophic marine environment (Alboran Sea, Western Mediterranean).Crossref | GoogleScholarGoogle Scholar | 12024265PubMed |

Alonso-Sáez, L., Arístegui, J., Pinhassi, J., Gómez-Consarnau, L., González, J. M., Vaqué, D., Agustí, S., and Gasol, J. M. (2007). Bacterial assemblage structure and carbon metabolism along a productivity gradient in the NE Atlantic Ocean. Aquatic Microbial Ecology 46, 43–53.
Bacterial assemblage structure and carbon metabolism along a productivity gradient in the NE Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Azam, F. (1998). Microbial control of oceanic carbon flux: the plot thickens. Science 280, 694–696.
Microbial control of oceanic carbon flux: the plot thickens.Crossref | GoogleScholarGoogle Scholar |

Baudoux, A. C., Veldhuis, M. J. W., Witte, H. J., and Brussaard, C. P. D. (2007). Viruses as mortality agents of picophytoplankton in the deep chlorophyll maximum layer during IRONAGES III. Limnology and Oceanography 52, 2519–2529.
Viruses as mortality agents of picophytoplankton in the deep chlorophyll maximum layer during IRONAGES III.Crossref | GoogleScholarGoogle Scholar |

Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., Rudolf, V. H. W., Schreiber, S. J., Urban, M. C., and Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in Ecology & Evolution 26, 183–192.
Why intraspecific trait variation matters in community ecology.Crossref | GoogleScholarGoogle Scholar |

Bouvier, T., Del Giorgio, P. A., and Gasol, J. M. (2007). A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems. Environmental Microbiology 9, 2050–2066.
A comparative study of the cytometric characteristics of high and low nucleic-acid bacterioplankton cells from different aquatic ecosystems.Crossref | GoogleScholarGoogle Scholar | 17635549PubMed |

Bouvy, M., Bettarel, Y., Bouvier, C., Domaizon, I., Jacquet, S., Le Floc’h, E., Montanié, H., Mostajir, B., Sime-Ngando, T., Torréton, J. P., Vidussi, F., and Bouvier, T. (2011). Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change. Environmental Microbiology 13, 1842–1857.
Trophic interactions between viruses, bacteria and nanoflagellates under various nutrient conditions and simulated climate change.Crossref | GoogleScholarGoogle Scholar | 21605305PubMed |

Breitbart, M. (2012). Marine viruses: truth or dare. Annual Review of Marine Science 4, 425–448.
Marine viruses: truth or dare.Crossref | GoogleScholarGoogle Scholar | 22457982PubMed |

Brum, J. R., Hurwitz, B. L., Schofield, O., Ducklow, H. W., and Sullivan, M. B. (2016). Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. The ISME Journal 10, 437–449.
Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics.Crossref | GoogleScholarGoogle Scholar | 26296067PubMed |

Brussaard, C. P. (2004). Optimisation of procedures for counting viruses by flow cytometry. Applied and Environmental Microbiology 70, 1506–1513.
Optimisation of procedures for counting viruses by flow cytometry.Crossref | GoogleScholarGoogle Scholar | 15006772PubMed |

Burdige, D. J., Komada, T., Magen, C., and Chanton, J. P. (2016). Carbon cycling in Santa Barbara Basin sediments: a modeling study. Journal of Marine Research 74, 133–159.
Carbon cycling in Santa Barbara Basin sediments: a modeling study.Crossref | GoogleScholarGoogle Scholar |

Cappello, S., Genovese, M., Della Torre, C., Crisari, A., Hassanshahian, M., Santisi, S., Calogero, R., and Yakimova, M. M. (2012). Effect of bioemulsificant exopolysaccharide (EPS2003) on microbial community dynamics during assays of oil spill bioremediation: a microcosm study. Marine Pollution Bulletin 64, 2820–2828.
Effect of bioemulsificant exopolysaccharide (EPS2003) on microbial community dynamics during assays of oil spill bioremediation: a microcosm study.Crossref | GoogleScholarGoogle Scholar | 23067540PubMed |

De Corte, D., Sintes, E., Yokokawa, T., Lekunberri, I., and Herndl, G. J. (2016). Large-scale distribution of microbial and viral populations in the South Atlantic Ocean. Environmental Microbiology Reports 8, 305–315.
Large-scale distribution of microbial and viral populations in the South Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar | 26765966PubMed |

Ding, Y., Bao, X. W., Yao, Z. G., Song, D. H., Song, J., Gao, J., and Li, J. Y. (2018). Effect of coastal-trapped waves on the synoptic variations of the Yellow Sea Warm Current during winter. Continental Shelf Research 167, 14–31.
Effect of coastal-trapped waves on the synoptic variations of the Yellow Sea Warm Current during winter.Crossref | GoogleScholarGoogle Scholar |

Falcioni, T., Papa, S., and Gasol, J. M. (2008). Evaluating the flow-cytometric nucleic acid double-staining protocol in realistic situations of planktonic bacterial death. Applied and Environmental Microbiology 74, 1767–1779.
Evaluating the flow-cytometric nucleic acid double-staining protocol in realistic situations of planktonic bacterial death.Crossref | GoogleScholarGoogle Scholar | 18223113PubMed |

Fuhrman, J. A., and Noble, R. T. (1995). Viruses and protists cause similar bacterial mortality in coastal seawater. Limnology and Oceanography 40, 1236–1242.
Viruses and protists cause similar bacterial mortality in coastal seawater.Crossref | GoogleScholarGoogle Scholar |

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. Scientia Marina 64, 197–224.
Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities.Crossref | GoogleScholarGoogle Scholar |

Gasol, J. M., Zweifel, U. L., Peters, F., Fuhrman, J. A., and Hagström, A. (1999). Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria. Applied and Environmental Microbiology 65, 4475–4483.
Significance of size and nucleic acid content heterogeneity as measured by flow cytometry in natural planktonic bacteria.Crossref | GoogleScholarGoogle Scholar | 10508078PubMed |

Guixa-Boixereu, N., Vasqué, D., Gasol, J. P., and Pedrós-Alió, C. (1999). Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system. Aquatic Microbial Ecology 19, 205–213.
Distribution of viruses and their potential effect on bacterioplankton in an oligotrophic marine system.Crossref | GoogleScholarGoogle Scholar |

Hara, S., Terauchi, K., and Koike, I. (1991). Abundance of viruses in marine waters: assessment by epifluorescence and transmission electron microscopy. Applied and Environmental Microbiology 57, 2731–2734.
Abundance of viruses in marine waters: assessment by epifluorescence and transmission electron microscopy.Crossref | GoogleScholarGoogle Scholar | 16348556PubMed |

Herlemann, D. P., Labrenz, M., Jürgens, K., Bertilsson, S., Waniek, J. J., and Andersson, A. F. (2011). Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. The ISME Journal 5, 1571–1579.
Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea.Crossref | GoogleScholarGoogle Scholar | 21472016PubMed |

Hobbie, J. E., Daley, R. J., and Jasper, S. (1977). Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied and Environmental Microbiology 33, 1225–1228.
Use of nuclepore filters for counting bacteria by fluorescence microscopy.Crossref | GoogleScholarGoogle Scholar | 327932PubMed |

Hung, C. W., Huang, K. H., Shih, Y. Y., Lin, Y. S., Chen, H. H., Wang, C. C., Ho, C. Y., Hung, C. C., and Burdige, D. J. (2016). Benthic fluxes of dissolved organic carbon from gas hydrate sediments in the northern South China Sea. Scientific Reports 6, 29597.
Benthic fluxes of dissolved organic carbon from gas hydrate sediments in the northern South China Sea.Crossref | GoogleScholarGoogle Scholar | 27432631PubMed |

Jiao, N. Z., Zhao, Y. L., Luo, T. W., and Wang, S. L. (2006). Natural and anthropogenic forcing on the dynamics of virioplankton in the Yangtze river estuary. Journal of the Marine Biological Association of the United Kingdom 86, 543–550.
Natural and anthropogenic forcing on the dynamics of virioplankton in the Yangtze river estuary.Crossref | GoogleScholarGoogle Scholar |

Junger, P. C., Amado, A. M., Paranhos, R., Cabral, A. S., Jacques, S. M., and Farjalla, V. F. (2017). Salinity drives the virioplankton abundance but not production in tropical coastal lagoons. Microbial Ecology 75, 1–12.
Salinity drives the virioplankton abundance but not production in tropical coastal lagoons.Crossref | GoogleScholarGoogle Scholar |

Karuza, A., Celussi, M., Cibic, T., Del Negro, P., and De Vittor, C. (2012). Virioplankton and bacterioplankton in a shallow CO2-dominated hydrothermal vent (Panarea Island, Tyrrhenian Sea). Estuarine, Coastal and Shelf Science 97, 10–18.
Virioplankton and bacterioplankton in a shallow CO2-dominated hydrothermal vent (Panarea Island, Tyrrhenian Sea).Crossref | GoogleScholarGoogle Scholar |

Kong, X. P., and Ye, S. H. (2014). The impact of water temperature on water quality indexes in north of Liaodong Bay. Marine Pollution Bulletin 80, 245–249.
The impact of water temperature on water quality indexes in north of Liaodong Bay.Crossref | GoogleScholarGoogle Scholar |

Kopylov, A. I., Kosolapov, D. B., and Zabotkina, E. A. (2011). Impact of viruses on heterotrophic bacterioplankton and Picocyanobacteria in reservoirs. Doklady Biological Sciences 437, 91–93.
Impact of viruses on heterotrophic bacterioplankton and Picocyanobacteria in reservoirs.Crossref | GoogleScholarGoogle Scholar | 21562954PubMed |

Larsen, J. B., Larsen, A., Thyrhaug, R., Bratbak, G., and Sandaa, R. A. (2008). Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO2 levels. Biogeosciences 5, 523–533.
Response of marine viral populations to a nutrient induced phytoplankton bloom at different pCO2 levels.Crossref | GoogleScholarGoogle Scholar |

Lehtoranta, J., Savchuk, O. P., Elken, J., Dahlbo, K., Kuosa, H., Raateoja, M., Kauppila, M., Räike, A., and Pitkänen, H. (2017). Atmospheric forcing controlling inter-annual nutrient dynamics in the open Gulf of Finland. Journal of Marine Systems 171, 4–20.
Atmospheric forcing controlling inter-annual nutrient dynamics in the open Gulf of Finland.Crossref | GoogleScholarGoogle Scholar |

Li, W. K. W., and Dickie, P. M. (2001). Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal inlet (Bedford Basin) by flow cytometry. Cytometry: The Journal of the International Society for Analytical Cytology 44, 236–246.
Monitoring phytoplankton, bacterioplankton, and virioplankton in a coastal inlet (Bedford Basin) by flow cytometry.Crossref | GoogleScholarGoogle Scholar |

Li, Y. F., Guo, L., and Feng, H. (2015). Status and trends of sediment metal pollution in Bohai Sea, China. Current Pollution Reports 1, 191–202.
Status and trends of sediment metal pollution in Bohai Sea, China.Crossref | GoogleScholarGoogle Scholar |

Liao, C. Y., and Kannan, K. (2019). Species-specific accumulation and temporal trends of bisphenols and benzophenones in mollusks from the Chinese Bohai Sea during 2006–2015. Science of The Total Environment 653, 168–175.
Species-specific accumulation and temporal trends of bisphenols and benzophenones in mollusks from the Chinese Bohai Sea during 2006–2015.Crossref | GoogleScholarGoogle Scholar |

Lin, X. P., Yang, J. Y., Guo, J. S., Zhang, Z. X., Yin, Y. Q., Song, X. Z., and Zhang, X. H. (2011). An asymmetric upwind flow, Yellow Sea Warm Current: 1. New observations in the western Yellow Sea. Journal of Geophysical Research. Oceans 116, C04026.
An asymmetric upwind flow, Yellow Sea Warm Current: 1. New observations in the western Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Lips, U., Laanemets, J., Lips, I., Liblik, T., Suhhova, I., and Suursaar, Ü. (2017). Wind-driven residual circulation and related oxygen and nutrient dynamics in the Gulf of Finland (Baltic Sea) in winter. Estuarine, Coastal and Shelf Science 195, 4–15.
Wind-driven residual circulation and related oxygen and nutrient dynamics in the Gulf of Finland (Baltic Sea) in winter.Crossref | GoogleScholarGoogle Scholar |

Liu, X., Chiang, K. P., Liu, S. M., Wei, H., Zhao, Y., and Huang, B. Q. (2015). Influence of the Yellow Sea Warm Current on phytoplankton community in the central Yellow Sea. Deep-sea Research. Part I, Oceanographic Research Papers 106, 17–29.
Influence of the Yellow Sea Warm Current on phytoplankton community in the central Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Lü, L. G., Wang, X., Wang, H., Li, L., and Yang, G. (2013). The variations of zooplankton biomass and their migration associated with the Yellow Sea Warm Current. Continental Shelf Research 64, 10–19.
The variations of zooplankton biomass and their migration associated with the Yellow Sea Warm Current.Crossref | GoogleScholarGoogle Scholar |

Lymer, D., and Vrede, K. (2006). Nutrient additions resulting in phage release and formation of non-nucleoid-containing bacteria. Aquatic Microbial Ecology 43, 107–112.
Nutrient additions resulting in phage release and formation of non-nucleoid-containing bacteria.Crossref | GoogleScholarGoogle Scholar |

Ma, J., Qiao, F. L., Xia, C. S., and Kim, C. S. (2006). Effects of the Yellow Sea Warm Current on the winter temperature distribution in a numerical model. Journal of Geophysical Research. Oceans 111, 1–12.
Effects of the Yellow Sea Warm Current on the winter temperature distribution in a numerical model.Crossref | GoogleScholarGoogle Scholar |

Mojica, K. D., and Brussaard, C. P. (2014). Factors affecting virus dynamics and microbial host–virus interactions in marine environments. FEMS Microbiology Ecology 89, 495–515.
Factors affecting virus dynamics and microbial host–virus interactions in marine environments.Crossref | GoogleScholarGoogle Scholar | 24754794PubMed |

Murray, A. G., and Jackson, G. A. (1992). Viral dynamics: a model of the effects of size, shape, motion and abundance of single-celled planktonic organisms and other particles. Marine Ecology Progress Series 89, 103–116.
Viral dynamics: a model of the effects of size, shape, motion and abundance of single-celled planktonic organisms and other particles.Crossref | GoogleScholarGoogle Scholar |

Paerl, H. W., and Huisman, J. (2008). Climate. Blooms like it hot. Science 320, 57–58.
Climate. Blooms like it hot.Crossref | GoogleScholarGoogle Scholar | 18388279PubMed |

Pan, L. A., Zhang, J., and Zhang, L. H. (2007). Picophytoplankton, nanophytoplankton, heterotrohpic bacteria and viruses in the Changjiang Estuary and adjacent coastal waters. Journal of Plankton Research 29, 187–197.
Picophytoplankton, nanophytoplankton, heterotrohpic bacteria and viruses in the Changjiang Estuary and adjacent coastal waters.Crossref | GoogleScholarGoogle Scholar |

Paterson, J. S., Nayar, S., Mitchell, J. G., and Seuront, L. (2012). A local upwelling controls viral and microbial community structure in South Australian continental shelf waters. Estuarine, Coastal and Shelf Science 96, 197–208.
A local upwelling controls viral and microbial community structure in South Australian continental shelf waters.Crossref | GoogleScholarGoogle Scholar |

Proctor, L. M., and Fuhrman, J. A. (1990). Viral mortality of marine bacteria and cyanobacteria. Nature 343, 60–62.
Viral mortality of marine bacteria and cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Sandaa, R. A., Gómez-Consarnau, L., Pinhassi, J., Riemann, L., Malits, A., Weinbauer, M. G., Gasol, J. M., and Thingstad, T. F. (2009). Viral control of bacterial biodiversity-evidence from a nutrient-enriched marine mesocosm experiment. Environmental Microbiology 11, 2585–2597.
Viral control of bacterial biodiversity-evidence from a nutrient-enriched marine mesocosm experiment.Crossref | GoogleScholarGoogle Scholar | 19558511PubMed |

Seymour, J. R., Seuront, L., Doubell, M., Waters, R. L., and Mitchell, J. G. (2006). Microscale patchiness of virioplankton. Journal of the Marine Biological Association of the United Kingdom 86, 551–561.
Microscale patchiness of virioplankton.Crossref | GoogleScholarGoogle Scholar |

Song, D. H., Bao, X. W., Wang, X. H., Xu, L. L., Lin, X. P., and Wu, D. X. (2009). The inter-annual variability of the Yellow Sea Warm Current surface axis and its influencing factors. Chinese Journal of Oceanology and Limnology 27, 607–613.
The inter-annual variability of the Yellow Sea Warm Current surface axis and its influencing factors.Crossref | GoogleScholarGoogle Scholar |

Sorensen, G. (2009). The role of the virus–phytoplankton system in marine biogeochemical cycling: possible impacts of climate change. The Plymouth Student Scientist 2, 289–302.

Sun, S. (2012). New perception of jellyfish bloom in the East China Sea and Yellow Sea. Oceanologia et Limnologia Sinica 43, 406–410.
New perception of jellyfish bloom in the East China Sea and Yellow Sea.Crossref | GoogleScholarGoogle Scholar |

Suttle, C. A. (1994). The significance of viruses to mortality in aquatic microbial communities. Microbial Ecology 28, 237–243.
The significance of viruses to mortality in aquatic microbial communities.Crossref | GoogleScholarGoogle Scholar | 24186450PubMed |

Suttle, C. A. (2005). Viruses in the sea. Nature 437, 356–361.
Viruses in the sea.Crossref | GoogleScholarGoogle Scholar | 16163346PubMed |

Suttle, C. A. (2007). Marine viruses: major players in the global ecosystem. Nature Reviews. Microbiology 5, 801–812.
Marine viruses: major players in the global ecosystem.Crossref | GoogleScholarGoogle Scholar | 17853907PubMed |

Tanaka, T., and Rassoulzadegan, F. (2004). Vertical and seasonal variations of bacterial abundance and production in the mesopelagic layer of the NW Mediterranean Sea: bottom-up and top-down controls. Deep-sea Research. Part I, Oceanographic Research Papers 51, 531–544.
Vertical and seasonal variations of bacterial abundance and production in the mesopelagic layer of the NW Mediterranean Sea: bottom-up and top-down controls.Crossref | GoogleScholarGoogle Scholar |

Teague, W. J., and Jacobs, G. A. (2000). Current observations on the development of the Yellow Sea Warm Current. Journal of Geophysical Research. Oceans 105, 3401–3411.
Current observations on the development of the Yellow Sea Warm Current.Crossref | GoogleScholarGoogle Scholar |

Thingstad, T. F., and Lignell, R. (1997). Theorical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquatic Microbial Ecology 13, 19–27.
Theorical models for the control of bacterial growth rate, abundance, diversity and carbon demand.Crossref | GoogleScholarGoogle Scholar |

Töpper, B., Thingstad, T. F., and Sandaa, R. A. (2013). Effects of differences in organic supply on bacterial diversity subject to viral lysis. FEMS Microbiology Ecology 83, 202–213.
Effects of differences in organic supply on bacterial diversity subject to viral lysis.Crossref | GoogleScholarGoogle Scholar | 22861500PubMed |

Wang, M., Liang, Y. T., Bai, X. G., Jiang, X. J., Wang, F., and Qiao, Q. (2010). Distribution of microbial populations and their relationship with environmental parameters in the coastal waters of Qingdao, China. Environmental Microbiology 12, 1926–1939.
Distribution of microbial populations and their relationship with environmental parameters in the coastal waters of Qingdao, China.Crossref | GoogleScholarGoogle Scholar | 20406288PubMed |

Wang, C. X., Wang, Y. B., Paterson, J. S., Michell, J. G., Hu, X. K., Zhang, H., and Sheng, Y. Q. (2016). Macroscale distribution of virioplankton and heterotrophic bacteria in the Bohai Sea. FEMS Microbiology Ecology 92, fiw017.
Macroscale distribution of virioplankton and heterotrophic bacteria in the Bohai Sea.Crossref | GoogleScholarGoogle Scholar |

Wei, W., Zhang, R., Peng, L. L., Liang, Y. T., and Jiao, N. Z. (2018). Effects of temperature and photosynthetically active radiation on virioplankton decay in the western Pacific Ocean. Scientific Reports 8, 1525.
Effects of temperature and photosynthetically active radiation on virioplankton decay in the western Pacific Ocean.Crossref | GoogleScholarGoogle Scholar | 29367730PubMed |

Weinbauer, M. G. (2004). Ecology of prokaryotic viruses. FEMS Microbiology Reviews 28, 127–181.
Ecology of prokaryotic viruses.Crossref | GoogleScholarGoogle Scholar | 15109783PubMed |

Wilhelm, S. W., and Suttle, C. A. (1999). Viruses and nutrient cycles in the sea. Bioscience 49, 781–788.
Viruses and nutrient cycles in the sea.Crossref | GoogleScholarGoogle Scholar |

Winter, C., Bouvier, T., Weinbauer, M. G., and Thingstad, T. F. (2010). Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner hypothesis’ revisited. Microbiology and Molecular Biology Reviews 74, 42–57.
Trade-offs between competition and defense specialists among unicellular planktonic organisms: the ‘killing the winner hypothesis’ revisited.Crossref | GoogleScholarGoogle Scholar | 20197498PubMed |

Winter, C., Payet, J. P., and Suttle, C. A. (2012). Modeling the winter-to-summer transition of prokaryotic and viral abundance in the Arctic Ocean. PLoS One 7, e52794.
Modeling the winter-to-summer transition of prokaryotic and viral abundance in the Arctic Ocean.Crossref | GoogleScholarGoogle Scholar | 23285186PubMed |

Wu, Q. L., Zwart, G., Schauer, M., Agterveld, M. P. K., and Hahn, M. W. (2006). Bacterioplankton community composition along a salinity gradient of sixteen high mountain lakes located on the Tibetan Plateau, China. Applied and Environmental Microbiology 72, 5478–5485.
Bacterioplankton community composition along a salinity gradient of sixteen high mountain lakes located on the Tibetan Plateau, China.Crossref | GoogleScholarGoogle Scholar | 16885301PubMed |

Xu, L. L., Wu, D. X., Lin, X. P., and Ma, C. (2009). The study of the yellow sea warm current and its seasonal variability. Journal of Hydrodynamics. Ser. B 21, 159–165.
The study of the yellow sea warm current and its seasonal variability.Crossref | GoogleScholarGoogle Scholar |

Zar, J. H. (2009). ‘Biostatistical Analysis.’ 5th edn. (Prentice Hall: Upper Saddle River, NJ, USA.)