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Occurrence and role of virioplankton in a tropical estuarine system

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Abstract

Only a few studies have reported on viral dynamics in estuarine environments, and the factors regulating viral ecology are not well known. We herein aimed to address the factors controlling virus–host relationships in tropical estuaries. To accomplish this, we combine a historical data series (2011–2017), containing virus and prokaryote abundances, with environmental data from Guanabara Bay, Brazil. Water quality gradients and tides were found to regulate the structure of prokaryotic communities, and seasonal patterns added complexity to the dynamics of viral populations. Prediction models showed a balance between expected and recorded virus–host relationships. However, changes in virus-microbial ratio (VMR) were found in areas with microorganism increases and regions showing critical environmental changes. Our results demonstrated that VMR changes are multifactorial and cannot be associated with any specific factor. Neither Kill-the-Winner nor Piggyback-the-Winner models can predict VMR in a highly dynamic environment strongly influenced by eutrophication. In sum, it can be concluded that special care is necessary when analyzing models for predicting virus and host abundances, as ecological factors control host distribution and play a significant role in the virus–host relationship.

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References

  • Andrade, L., A. M. Gonzalez, F. V. Araujo & R. Paranhos, 2003. Flow cytometry assessment of bacterioplankton in tropical marine environments. Journal of Microbiological Methods 55: 841–850.

    CAS  PubMed  Google Scholar 

  • Angly, F. E., B. Felts, M. Breitbat, P. Salamon, R. A. Edwards, C. Carlson, A. M. Chan, M. Haynes, S. Kelley, H. Liu, J. M. Mahaffy, J. E. Mueller, J. Nulton, R. Olson, R. Parsons, S. Rayhawk, C. A. Suttle & F. Rohwer, 2006. The marine viromes of four oceanic regions. PloS Biology 4: 2121–2131.

    CAS  Google Scholar 

  • Auguet, J. C., H. Montanié, D. Delmas, H. J. Hartmann & V. Huet, 2005. Dynamic of virioplankton abundance and its environmental control in the Charente estuary (France). Microbial Ecology 50: 337–349.

    CAS  PubMed  Google Scholar 

  • Auguet, J. C., H. Montanié, H. J. Hartmann, P. Lebaron, E. O. Casamayor, P. Catala & D. Delmas, 2009. Potential effect of freshwater virus on the structure and activity of bacterial communities in the Marennes-Oléron Bay (France). Microbial Ecology 57: 295–306.

    CAS  PubMed  Google Scholar 

  • Bergh, O., K. Y. Borsheim, G. Bratbak & M. Heldal, 1989. High abundance of viruses found in aquatic environments. Nature 340: 467–468.

    CAS  PubMed  Google Scholar 

  • Bettarel, Y., R. Arfi, T. Bouvier, M. Bouvy, E. Briand, J. Colombet, D. Corbin & T. Sime-Ngando, 2008. Virioplankton distribution and activity in a tropical eutrophicated bay. Estuarine, Coastal and Shelf Science 80: 425–429.

    Google Scholar 

  • Bettarel, Y., T. Bouvier, M. Agis, C. Bouvier, et al., 2011. Viral distribution and life strategies in the Bach Dang estuary, Vietnam. Microbial Ecology 62: 143–154.

    PubMed  Google Scholar 

  • Bonilla-Findji, O., A. Malits, D. Lefèvre, E. Rochelle-Newall, R. Lemée, M. G. Weinbauer & J. P. Gattuso, 2008. Viral effects on bacterial respiration, production and growth efficiency: consistent trends in the Southern Ocean and the Mediterranean Sea. Deep-Sea Research Part II: Topical Studies in Oceanography 55: 790–800.

    Google Scholar 

  • Bratbak, G. & M. Heldal, 1995. Molecular ecology of aquatic microbes. In Joint, I. (ed.), Viruses: The New Players in the Game; Their Ecological Role and Could They Mediate Genetic Exchange by Transduction. Springer, Heidelberg: 249–264.

    Google Scholar 

  • Breitbart, M., 2012. Marine viruses: truth or dare. Annual Review of Marine Science 4: 425–448.

    PubMed  Google Scholar 

  • Brum, J. R. & M. Sullivan, 2015. Rising to the challenge: accelerated pace of discovery transforms marine virology. Nature 13: 147–159.

    CAS  Google Scholar 

  • Brum, J., B. L. Hurwitz, O. Schofield, H. W. Ducklow & M. B. Sullivan, 2015. Seasonal time bombs: dominant temperate viruses affect Southern Ocean microbial dynamics. ISME Journal 10: 437–449.

    PubMed  Google Scholar 

  • Brussaard, C., 2004. Optimization of procedures for counting viruses by flow cytometry. Applied and Environmental Microbiology 70: 1506–1513.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brussaard, C. P. D., W. W. Steven, F. Thingstad, M. G. Weinbauer, G. Bratbak, M. Heldal, S. A. Kimmance, M. Middelboe, K. Nagasaki, J. H. Paul, D. C. Schroeder, C. A. Suttle, D. Vaqué & K. E. Wommack, 2008a. Global-scale processes with a nanoscale drive: the role of marine viruses. ISME Journal 20: 575–578.

    Google Scholar 

  • Brussaard, C. P. D., K. R. Timmermans, J. Uitz & M. J. W. Veldhuis, 2008b. Virioplankton dynamics and virally induced phytoplankton lysis versus microzooplankton grazing southeast of the Kerguelen (Southern Ocean). Deep-Sea Research Part II 55: 752–765.

    Google Scholar 

  • Cabral, A. S., M. M. Lessa, P. C. Junger, F. L. Thompson & R. Paranhos, 2017. Virioplankton dynamics are related to eutrophication levels in a tropical urbanized bay. Plos ONE 12: e0174653.

    PubMed  PubMed Central  Google Scholar 

  • Cael, B. B., M. C. G. Carlson, C. L. Follet & M. J. Follows, 2018. Marine virus-like particles and microbes: a linear interpretation. Frontiers in Microbiology 9: 1–4.

    Google Scholar 

  • Cai, L., R. Zhang, Y. He, X. Feng & N. Jiao, 2016. Metagenomic analysis of virioplankton of the subtropical Jiulong River estuary, China. Viruses 8: 35–48.

    PubMed Central  Google Scholar 

  • Chen, X., W. Wei, J. Wang, H. Li, J. Sun, R. Ma, N. Jiao & R. Zhang, 2019. Tide driven microbial dynamics through virus–host interactions in the estuarine ecosystem. Water Research 160: 118–129.

    CAS  PubMed  Google Scholar 

  • Cissoko, M. M., A. Desnues, M. Bouvy, T. Sime-Ngando, E. Verling & Y. Bettarel, 2008. Effects of freshwater and seawater mixing on vireo and bacterioplancton in a tropical estuary. Freshwater Biology 53: 1154–1162.

    Google Scholar 

  • Coutinho, F. H., C. B. Silveira, G. B. Gregoracci, C. C. Thompson, R. A. Edwards, C. P. D. Brussaard, B. E. Dutilh & F. L. Thompson, 2017. Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans. Nature Communications 8: 15955.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Coutinho, F. H., C. C. Thompson, A. S. Cabral, R. Paranhos, B. E. Dutilh & F. L. Thompson, 2019. Modelling the influence of environmental parameters over marine planktonic microbial communities using artificial neural networks. Science of the Total Environment 677: 205–214.

    CAS  PubMed  Google Scholar 

  • Danovaro, R., C. Corinaldesi, et al., 2011. Marine viruses and global change. FEMS Microbiology Reviews 35: 993–1034.

    CAS  PubMed  Google Scholar 

  • Davidson, K., R. J. Gowen, P. J. Harrison, L. E. Fleming, P. Hoagland & G. Moschonas, 2014. Anthropogenic nutrients and harmful algae in coastal waters. Journal of Environmental Management 146: 206–216.

    CAS  PubMed  Google Scholar 

  • De Corte, D., E. Sintes, T. Yokokawa, I. Lekunberri & G. J. Herndl, 2016. Large-scale distribution of microbial and viral populations in the South Atlantic Ocean. Environ Microbiol Rep. 8(2): 305–315.

    PubMed  PubMed Central  Google Scholar 

  • Evans, C., J. Brandsma, D. W. Pond, H. J. Venables, M. P. Meredith, H. J. Witte, S. Stammerjohn, W. H. Wilson, A. Clarke & C. P. D. Brussaard, 2017. Drivers of interannual variability in virioplankton abundance at the coastal western Antarctic peninsula and the potential effects of climate change. Environmental Microbiology 19: 740–755.

    CAS  PubMed  Google Scholar 

  • Fernández, L., A. Rodríguez & P. García, 2018. Phage or foe: an insight into the impact of viral predation on microbial communities. ISME Journal 12: 1171–1179.

    PubMed  Google Scholar 

  • Fistarol, G. O., F. H. Coutinho, A. P. B. Moreira, T. Venas, A. Cánovas, S. E. M. de Paula, R. L. de Coutinho, J. L. Moura, D. R. Valentin, R. Tenenbaum, R. A. B. Paranhos, et al., 2015. Environmental and sanitary conditions of Guanabara Bay, Rio de Janeiro. Frontiers Microbiology 6: 1–17.

    Google Scholar 

  • Fonseca, E. M., J. A. Baptista Neto, C. G. Silva, J. J. McAlister, B. J. Smith & M. A. Fernandez, 2013. Stormwater impact in Guanabara Bay (Rio de Janeiro): evidences of seasonal variability in the dynamic of the sediment heavy metals. Estuarine, Coastal and Shelf Science 130: 161–168.

    CAS  Google Scholar 

  • Gasol, J. M. & P. A. del Giogio, 2000. Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Scientia Marina 64: 197–224.

    Google Scholar 

  • Glibert, P. M., J. Harrison, C. Heil & S. Seitzinger, 2006. Escalating worldwide use of urea: a global change contributing to coastal eutrophication. Biogeochemistry 77: 441–463.

    CAS  Google Scholar 

  • Grasshoff, K., M. Erhardt & K. Kremling, 1999. Methods of Seawater Analysis. Wiley, Weinhein.

    Google Scholar 

  • Greening, H., A. Janicki, E. T. Sherwood, R. Pribble & J. O. R. Johansson, 2014. Ecosystem responses to long-term nutrient management in an urban estuary: tampa Bay, Florida, USA. Estuarine, Coastal and Shelf Science 151: 1–16.

    Google Scholar 

  • Greenwood, N., D. J. Hydes, C. Mahaffey, A. Wither, J. Barry, D. B. Sivyer, D. J. Pearce, S. E. Hartman, O. Andres & H. E. Lees, 2011. Spatial and temporal variability in nutrient concentrations in Liverpool Bay, a temperate latitude region of freshwater influence. Ocean Dynamics 61: 2181–2199.

    Google Scholar 

  • Gregoracci, G. B., J. R. Nascimento, A. S. Cabral, R. Paranhos, J. L. Valentin, C. Thompson & F. L. Thompson, 2012. Structuring of bacterioplankton diversity in a large tropical bay. PLos ONE 7: e31408.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Halpern, B. S., M. Frazier, J. Potapenko, K. S. Casey, K. Koenig, C. Longo, J. S. Lowndes, R. C. Rockwood, E. R. Selig, K. A. Selkoe & S. Walbridge, 2015. Spatial and temporal changes in cumulative human impacts on the world’s ocean. Nature Communications 6: 7615.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hewson, I., et al., 2001. Effects of concentrated viral communities on photosynthesis and community composition of co-occurring benthic microalgae and phytoplankton. Limnology and Oceanography 46: 1734–1746.

    Google Scholar 

  • Jacquet, S., T. Miki, R. Noble, P. Peduzzi & S. Wilhelm, 2010. Viruses in aquatic ecosystems: important advancements of the last 20 years and prospects for the future in the field of microbial oceanography and limnology. Advances in Oceanography and Limnology 1: 97–141.

    CAS  Google Scholar 

  • Jasna, V., A. Parvathi, V. K. Aswathy, S. Aparna, M. Dayana, A. J. Aswathy & N. V. Madhu, 2019. Factors determining variations in viral abundance and viral production in a tropical estuary influenced by monsoonal cycles. Regional Studies in Marine Science 28: 100589.

    Google Scholar 

  • Jasna, V., A. Parvathi, A. S. P. Ram, K. K. Balachandran, N. V. Madhu, M. Nair, R. Jyothibabu, V. Jayalakshmy, C. Revichandran & T. Sime-Ngando, 2017. Viral-induced mortality of prokaryotes in a tropical monsoonal estuary. Estuary Frontiers in Microbiology 8: 895.

    PubMed  Google Scholar 

  • Jasna, V., A. S. P. Ram, A. Parvathi & T. Sime-Ngando, 2018. Differential impact of lytic viruses on prokaryotic morphopopulations in a tropical estuarine system (Cochin estuary, India). Plos ONE 13: e0194020.

    PubMed  PubMed Central  Google Scholar 

  • Jiao, N., G. J. Herndl, D. A. Hansell, R. Benner, G. Kattner, S. W. Wilhelm, D. L. Kirchman, M. G. Weinbauer, T. Luo, F. Chen & F. Azam, 2010. Microbial production of recalcitrant dissolved organic matter: long-term carbon storage in the global ocean. Nature Reviews Microbiology 8: 593–599.

    CAS  PubMed  Google Scholar 

  • Jiao, N., Y. Zhao, T. Luo & X. Wang, 2006. Natural and anthropogenic forcing on the dynamics of virloplankton in the Yangtze River estuary. Journal of the Marine Biological Association of the United Kingdom 86: 543–550.

    Google Scholar 

  • Kauffman, G. J. & A. C. Belden, 2010. Water quality trends (1970 to 2005) along Delaware streams in the Delaware and Chesapeake Bay watersheds, USA. Water, Air, and Soil Pollution 208: 345–375.

    CAS  Google Scholar 

  • Kirchman, D., 2008. Microbial Ecology of the Oceans. Wiley, New Jersey.

    Google Scholar 

  • Knowles, B., B. Bailey, L. Boling, M. Breitbart, A. Cobián-Güemes, J. Del Campo, R. Edwards, B. Felts, J. Grasis, A. F. Haas, P. Katira, L. W. Kelly, A. Luque, J. Nulton, L. Paul, G. Peters, N. Robinett, S. Sandin, A. Segall, C. Silveira, M. Youle & F. Rohwer, 2017. Variability and host density independence in inductions-based estimates of environmental lysogeny. Nature Microbiology 2: 17064.

    CAS  PubMed  Google Scholar 

  • Knowles, B., C. B. Silveira, B. A. Bailey, K. Barott, V. A. Cantu, A. G. Cobián-Güemes, F. H. Coutinho, E. A. Dinsdale, B. Felts, K. A. Furby, E. E. George, K. T. Green, G. B. Gregoracci, A. F. Haas, J. M. Haggerty, E. R. Hester, N. Hisakawa, L. W. Kelly, Y. W. Lim, M. Little, A. Luque, T. McDole-Somera, K. McNair, L. S. de Oliveira, S. D. Quistad, N. L. Robinett, E. Sala, P. Salamon, S. E. Sanchez, S. Sandin, G. G. Z. Silva, J. Smith, C. Sullivan, C. Thompson, M. J. A. Vermeij, M. Youle, C. Young, B. Zgliczynski, R. Brainard, R. A. Edwards, J. Nulton, F. Thompson & F. Rohwer, 2016. Lytic to temperate switching of viral communities. Nature 531: 466–470.

    CAS  PubMed  Google Scholar 

  • Koonin, E. V. & Y. I. Wolf, 2012. Evolution of microbes and viruses: a paradigm shift in evolutionary biology? Frontiers in Cellular and Infection Microbiology 2: 119.

    PubMed  PubMed Central  Google Scholar 

  • Lennon, J. T. & J. B. H. Martiny, 2008. Rapid evolution buffers ecosystem impacts of viruses in a microbial food web. Ecology Letters. 11: 1178–1188.

    PubMed  Google Scholar 

  • Lewis, W. M., W. A. Wurtsbaugh & H. W. Paerl, 2011. Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environmental Science and Technology 45: 10300–10305.

    CAS  PubMed  Google Scholar 

  • Liu, J., Z. Hao, L. Ma, Y. Ji, M. Bartlam & Y. Wang, 2016. Spatio-temporal variations of high and low nucleic acid content bacteria in an exorheic river. PlosOne 11: e0153678.

    Google Scholar 

  • Maat, D. S., J. K. Crawfurd, K. R. Timmermans & C. P. D. Brussaard, 2014. Elevated CO2 and phosphate limitation favor Micromonas pusilla through stimulated growth and reduced viral impact. Applied and Environmental Microbiology 80: 3119–3127.

    PubMed  PubMed Central  Google Scholar 

  • Maranger, R. & D. F. Bird, 1995. Viral abundance in aquatic systems: a comparison between marine and fresh waters. Marine Ecology Progress Series 121: 217–226.

    Google Scholar 

  • Marie, D., N. Simon & D. Vaulot, 2005. Phytoplankton cell counting by flow cytometry. Elsevier, Oxford.

    Google Scholar 

  • Mayr, L. M., D. R. Tenenbaun, M. C. Villac, R. Paranhos, C. R. Nogueira, S. L. C. Bonecker & A. C. Bonecker, 1989. Hydrobiological characterization of Guanabara Bay. In Magoon, O. T. & C. Neves (eds), Coastlines of Brazil. American Society of Civil Engineers, New York: 124–139.

    Google Scholar 

  • Mojica, K. & C. Brussaard, 2014. Factors affecting virus dynamics and microbial host-virus interactions in marine environments. FEMS Microbiology Ecology 89: 495–515.

    CAS  PubMed  Google Scholar 

  • Mojica, K. D. A., J. Huisman, S. W. Wilhelm & C. Brussaard, 2016. Latitudinal variation in virus-induced mortality of phytoplankton across the North Atlantic Ocean. ISME Journal 10: 1–14.

    Google Scholar 

  • Monastersky, R., 2016. Meteorologists probe monster El Niño. Nature 529: 267–268.

    CAS  PubMed  Google Scholar 

  • Motegi, C., T. Nagata, T. Miki, M. G. Weinbauer, L. Legendre & F. Rassoulzadegand, 2009. Viral control of bacterial growth efficiency in marine pelagic environments. Limnology and Oceanography 54: 1901–1910.

    CAS  Google Scholar 

  • Nagata, T., C. Tamburini, J. Arístegui, F. Baltar, A. B. Bochdansky, S. FondaUmani, H. Fukuda, A. Gogou, D. A. Hansell, R. L. Hansman, G. J. Herndl, C. Panagiotopoulos, T. Reinthaler, R. Sohrin, P. Verdugo, N. Yamada, Y. Yamashita, T. Yokokawa & D. H. Bartlett, 2010. Emerging concepts on microbial processes in the bathypelagic ocean: ecology, biogeochemistry, and genomics. Deep-Sea Research Part II 57: 1519–1536.

    CAS  Google Scholar 

  • O’Malley, M. A., 2016. The ecological virus. Studies in History and Philosophy of Science Part C: Studies in History and Philosophy of Biological and Biomedical Sciences 59: 71–79.

    Google Scholar 

  • Obeng, N., A. A. Pratama & J. D. van Elsas, 2016. The significance of mutualistic phages for bacterial ecology and evolution. Trends in Microbiology 24: 440–449.

    CAS  PubMed  Google Scholar 

  • Ortmann, A., J. Lawrence & C. Suttle, 2002. Lysogeny and lytic viral production during a bloom of the cyanobacterium Synechococcus spp. Microbial Ecology 43: 225–231.

    CAS  PubMed  Google Scholar 

  • Paerl, H. W., 2009. Controlling eutrophication along the freshwater–marine continuum: dual nutrient (N and P) reductions are essential. Estuaries and Coasts 32: 593–601.

    CAS  Google Scholar 

  • Paerl, H. W., N. S. Hall, B. L. Peierls & K. L. Rossignol, 2014. Evolving paradigms and challenges in estuarine and coastal eutrophication dynamics in a culturally and climatically stressed world. Estuaries and Coasts 37: 243–258.

    Google Scholar 

  • Paranhos, R. & L. M. Mayr, 1993. Seasonal patterns of temperature and salinity in Guanabara Bay, Brazil. Fresenius Environmental Bulletin 2: 647–652.

    CAS  Google Scholar 

  • Paranhos, R., A. P. Pereira & L. M. Mayr, 1998. Diel variability of water quality in a pollution gradient in a tropical polluted bay. Environmental Monitoring Assessment 50: 131–141.

    CAS  Google Scholar 

  • Parikka, K. J., M. Le Romancer, N. Wauters & S. Jacquet, 2016. Deciphering the virus-to-prokaryote ratio (VPR): insights into virus–host relationships in a variety of ecosystems. Biological Reviews 1083: 1081–1100.

    Google Scholar 

  • Parsons, T. R., Y. Maita & C. M. Lalli, 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, Oxford.

    Google Scholar 

  • Parvathi, A., V. Jasna, K. C. Haridevi, S. Jina, M. Greeshma, J. Breezy & M. Nair, 2013. Diurnal variations in bacterial and viral production in Cochin estuary, India. Environmental Monitoring and Assessment 185: 8077–8088.

    CAS  PubMed  Google Scholar 

  • Payet, J. & C. Suttle, 2013. To kill or not to kill: the balance between lytic and lysogenic viral infection is driven by trophic status. Limnology and Oceanography 58: 465–474.

    Google Scholar 

  • Puxty, R. J., D. J. Evans, A. D. Millard & D. J. Scanlan, 2018. Energy limitation of cyanophage development: implications for marine carbon cycling. ISME Journal 12: 1273–1286.

    CAS  PubMed  Google Scholar 

  • Rohwer, F., D. Prangishvili & D. Lindell, 2009. Roles of viruses in the environment. Environmental Microbiology 11: 2771–2774.

    PubMed  Google Scholar 

  • R Core Team, 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Schiermeier, Q., 2015. Hunting the Godzilla El Niño. Nature 526: 490–491.

    CAS  PubMed  Google Scholar 

  • Seymour, J. R., L. Seuront, M. Doubell, R. L. Waters & J. G. Mitchell, 2006. Microscale patchiness of virioplankton. Journal of the Marine Biological Association of the United Kingdom 86: 551–561.

    Google Scholar 

  • Silveira, C. & F. Rohwer, 2016. Piggyback-the-Winner in host-associated microbial communities. NPJ Biofilms and Microbiomes 8: 881–890.

    Google Scholar 

  • Simon, M., H. P. Grossart, B. Schweitzer & H. Ploug, 2002. Microbial ecology of organic aggregates in aquatic ecosystems. Aquatic Microbial Ecology 28: 175–211.

    Google Scholar 

  • Spidlen, J., K. Breuer, C. Rosenberg, N. Kotecha & R. R. Brinkman, 2012. Flow repository: a resource of annotated flow cytometry datasets associated with peer-reviewed publications. Cytometry A 81: 727–731.

    PubMed  Google Scholar 

  • Solic, M. & N. Krstulovic, 1992. Separate and combined effects of solar radiation, temperature, salinity and pH on the survival of faecal coliforms in seawater. Marine Pollution Bulletin 24: 411–416.

    Google Scholar 

  • Suttle, C. A., 2007. Marine viruses—major players in the global ecosystem. Nature Reviews Microbiology 5: 801–812.

    CAS  PubMed  Google Scholar 

  • Suttle, C. A., 2005. Viruses in the sea. Nature 437: 356–361.

    CAS  PubMed  Google Scholar 

  • Thingstad, T., 2000. Elements of a theory for the mechanisms controlling abundance, diversity and biogeochemical role of lytic bacterial viruses in aquatic systems. Limnology and Oceanography 45: 1320–1328.

    Google Scholar 

  • Tsai, A., G. Gong, Y. Huang & C. Chao, 2015. Estimates of bacterioplâncton and Synechococcus spp. mortality from nanoflagellates grazing and viral lysis in the subtropical Danshui River estuary. Estuarine, Coastal and Shelf Science 153: 54–61.

    Google Scholar 

  • Valentin, J. L., D. R. Tenenbaum, A. C. T. Bonecker, S. L. C. Bonecker, C. R. Nogueira, R. Paranhos & M. C. Villac, 1999. Caractéristiques hydrobiologiques de la Baie de Guanabara (Rio de Janeiro, Brésil). Journal de Recherche Océanographique 24: 33–41.

    CAS  Google Scholar 

  • Vieira, R. P., A. M. Gonzalez, A. M. Cardoso, D. N. Oliveira, R. M. Albano, M. M. Clementino, O. B. Martins & R. Paranhos, 2008. Relationships between bacterial diversity and environmental variables in a tropical marine environment, Rio de Janeiro. Environmental Microbiology 10: 189–199.

    CAS  PubMed  Google Scholar 

  • Vila-Costa, M., J. M. Gasol, S. Sharma & M. A. Moran, 2012. Community analysis of high- and low-nucleic acid-containing bacteria in NW Mediterranean coastal waters using 16S rDNA pyrosequencing. Environmental Microbiology 6: 1390–1402.

    Google Scholar 

  • Wang, C., Y. Wang, J. S. Paterson, J. G. Mitchell, X. Hu, H. Zhang & Y. Sheng, 2016. Macroscale distribution of virioplankton and heterotrophic bacteria in the Bohai Sea. FEMS Microbiology Ecology 92: fiw017.

    PubMed  Google Scholar 

  • Wei, W., N. Wang, L. Cai, C. Zhang, N. Jiao & R. Zhang, 2019. Impacts of freshwater and seawater mixing on the production and decay of virioplankton in a subtropical estuary. Microbial Ecology 78: 843–854.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weitz, J. S. & S. W. Wilhelm, 2012. Ocean viruses and their effects on microbial communities and biogeochemical cycles. F1000 Biology Reports 4: 1–17.

    Google Scholar 

  • Weitz, J. S., S. J. Beckett, J. R. Brum, B. B. Cael & J. Dushoff, 2017. Lysis, lysogeny and virus-microbe ratios. Nature 549: 23295.

    Google Scholar 

  • West, M. & J. Harrison, 1997. Bayesian Forecasting and Dynamic Models, 2nd ed. Springer, New York.

    Google Scholar 

  • Wigington, C. H., D. Sonderegger, C. P. D. Brussaard, A. Buchan, J. F. Finke, J. A. Fuhrman, J. T. Lennon, M. Middelboe, C. A. Suttle, C. Stock, W. H. Wilson, K. E. Wommack, S. W. Wilhelm & J. S. Weitz, 2016. Re-examination of the relationship between marine virus and microbial cell abundances. Nature Microbiology 1: 15024.

    CAS  PubMed  Google Scholar 

  • Winget, D. M. & K. E. Wommack, 2009. Diel and daily fluctuations in virioplankton production in coastal ecosystems. Environmental Microbiology 11: 2904–2914.

    PubMed  Google Scholar 

  • Winget, D. M., R. R. Helton, K. E. Williamson, S. R. Bench, S. J. Williamson & K. E. Wommack, 2011. Repeating patterns of virioplankton production within an estuarine ecosystem. Proceedings of the National Academy of Sciences of the United States of America 108: 11506–11511.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wommack, K. E. & R. R. Colwell, 2000. Virioplankton: viruses in aquatic ecosystems. Microbiology and Molecular Biology Reviews 64: 69–114.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wommack, K. E., D. J. Nasko, J. Chopyk & G. E. Sakowski, 2015. Counts and sequences, observations that continue to change our understanding of viruses in nature. Journal of Microbiology 53: 181–192.

    CAS  Google Scholar 

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Acknowledgements

We are grateful to UFRJ Technological Park and the Pilot Association of Rio de Janeiro for providing access and logistics for sampling expeditions, respectively. This work is a contribution from the “Microbiological Observatory of Rio de Janeiro – MORio” funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Universal Grant No. 483.758/2010-8, and Research Fellowship Grant No. 312.949/2014-6), and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) (Research Aid APQ1 Grant Nos. 111.649/2011 and 110.586/2014) to RP. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001”. MML is grateful to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a Master’s scholarship (Graduate Program in Ecology - UFRJ). ASC received fellowships from CAPES (PNPD and Edital Ciências do Mar 09/2009), FAPERJ (E26/103.692/2012 – E26/201.775/2017) and CNPq (158537/2015-7). We also thank Mr. Dauro M. Garcia (Antônio Carlos Transportes Marítimos) for his professionalism and proactivity during expeditions, as well as the Hydrobiology Laboratory team for sampling, especially to Anderson A. dos Santos Junior for support in flow cytometry analysis. Finally, we would like to thank the anonymous reviewers and the Editor for their valuable suggestions.

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Cabral, A.S., Lessa, M.M., Mello, M.P. et al. Occurrence and role of virioplankton in a tropical estuarine system. Hydrobiologia 847, 4125–4140 (2020). https://doi.org/10.1007/s10750-020-04404-w

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