Not all viruses in nature are human enemies: a perspective on aquatic virus ecology in Brazil

Viruses cause various diseases in humans through vector-borne (e.g., Zika and dengue fever), airborne (e.g., measles) and water-borne (e.g., hepatitis) transmission, as well as direct physical contact (e.g., AIDS and herpes). Recently, the new coronavirus (SARS-CoV-2) pandemic has triggered the greatest global health crisis in a century. However, not all viruses in nature are human enemies. A vast body of literature indicates that viral infection is vital for ecosystem functioning by affecting nutrient cycling, controlling species growth and enhancing biodiversity. Here we provide a perspective on the ecological role of viruses in nature, with special focus on Brazilian aquatic ecosystems.

Keywords:
viral ecology; virioplankton; microorganisms; aquatic ecosystems; tropics

Authorship

Pedro Ciarlini Junger ^**e-mail: pedro.junger@gmail.com

Laboratório de Biodiversidade e Processos Microbianos – LMPB, Departamento de Hidrobiologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos – UFSCar, Rodovia Washington Luís, CEP 13565-905, São Carlos, SP, BrasilUniversidade Federal de São Carlos BrasilSão Carlos, SP, BrasilLaboratório de Biodiversidade e Processos Microbianos – LMPB, Departamento de Hidrobiologia, Centro de Ciências Biológicas e da Saúde, Universidade Federal de São Carlos – UFSCar, Rodovia Washington Luís, CEP 13565-905, São Carlos, SP, Brasil

https://orcid.org/0000-0001-8774-0738

Rafael Marques Almeida

Department of Ecology and Evolutionary Biology, Cornell University, 14853, Ithaca, NY, USACornell UniversityUSAIthaca, NY, USADepartment of Ecology and Evolutionary Biology, Cornell University, 14853, Ithaca, NY, USA

https://orcid.org/0000-0001-5398-7054

Raquel Mendonça

Laboratório de Ecologia Aquática, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Rua José Lourenço Kelmer, CEP 36036-900, Juiz de Fora, MG, BrasilUniversidade Federal de Juiz de ForaBrasilJuiz de Fora, MG, BrasilLaboratório de Ecologia Aquática, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Rua José Lourenço Kelmer, CEP 36036-900, Juiz de Fora, MG, Brasil

https://orcid.org/0000-0001-8731-8326

Vinicius Fortes Farjalla

Departamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, Av. Carlos Chagas Filho, 373, CEP 21941-590, Rio de Janeiro, RJ, BrasilUniversidade Federal do Rio de JaneiroBrasilRio de Janeiro, RJ, BrasilDepartamento de Ecologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro – UFRJ, Av. Carlos Chagas Filho, 373, CEP 21941-590, Rio de Janeiro, RJ, Brasil

https://orcid.org/0000-0003-4084-5983

Rossana Correa Netto de Melo

Laboratório de Biologia Celular, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Rua José Lourenço Kelmer, CEP 36036-900, Juiz de Fora, MG, BrasilUniversidade Federal de Juiz de ForaBrasilJuiz de Fora, MG, BrasilLaboratório de Biologia Celular, Departamento de Biologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora – UFJF, Rua José Lourenço Kelmer, CEP 36036-900, Juiz de Fora, MG, Brasil

https://orcid.org/0000-0003-1736-0806

Fábio Roland

https://orcid.org/0000-0001-8124-9972

Nathan Barros

https://orcid.org/0000-0003-1752-8621

*e-mail: pedro.junger@gmail.com

Associate Editors: André Megali Amado Joyce Andreia dos Santos, Simone Jaqueline Cardoso.

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (5)

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Figure 1
Viruses are extremely small (20-200 nm), smaller than bacterial cells (> 1000 nm), which in turn are smaller than animal and plant cells. nm = nanometer; μm = micrometer; cm = centimeter. Adapted from Melo (2018)MELO, R.C.N. Células & microscopia: princípios e práticas. 2. ed. Barueri: Manole, 2018, 300 p., with permission.

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Figure 2
Simplified illustration of the three main virus replication strategies: lytic cycle, lysogenic cycle and chronic infection.

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Figure 3
Image of an aquatic ecosystem bacterium infected with viruses, observed by transmission electron microscopy. The black “dots” indicate the presence of non-tailed bacteriophages in the bacterial cytoplasm. The boxed area shows a zoomed-in view of the structure of the viral protein capsule (capsid), composed of several repetitive morphological units (highlighted in blue). Image reproduced from Barros et al. (2010)BARROS, N., FARJALLA, V.F., SOARES, M.C., MELO, R.C.N. and ROLAND, F. Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake. Applied and Environmental Microbiology, 2010, 76(21), 7194-7201. http://dx.doi.org/10.1128/AEM.01161-10. PMid:20833790.
http://dx.doi.org/10.1128/AEM.01161-10... , with permission.

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Figure 4
Illustration of the effects of the “viral loop” on aquatic food webs. Viruses (A) break host cells, which are often unicellular organisms such as bacteria (B) and phytoplankton (C), thereby releasing nutrients (carbon, nitrogen and phosphorus; CNP) into the water. In this way, viruses divert the amount of carbon that would reach higher trophic levels, such as microzooplankton (flagellates and ciliates - D), macrozooplankton (rotifers, cladocerans and copepods - E) and predators (e.g., fish - F), and release them back to the base of aquatic food webs (B and C). The black arrows indicate the regular flow of carbon in aquatic food webs, whereas the red arrows indicate the flows mediated by viruses. The width of the red arrows roughly represents the magnitude of these flows based on the relative abundance and biomass of these organisms usually found in aquatic ecosystems. Note that this is a theoretical picture and the width of the arrows may change between specific ecosystems. Figure adapted from Farjalla et al. (2011)FARJALLA, V.F., AMADO, A.M. and ESTEVES, F.A. Bacterioplâncton. In: F.A. ESTEVES, ed. Fundamentos de limnologia. 3. ed. Rio de Janeiro: Interciência, 2011, pp. 355-373..

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Figure 5
Regression between viruses and bacterial counts from water samples collected in Brazilian aquatic ecosystems. The strong positive relationships (Amazon lakes: n = 66, r² = 0.84, p <0.01; Coastal lagoons: n = 18, r² = 0.39; p <0.01; Guanabara Bay: n = 246, r² = 0.53; p <0.01) indicate that high bacterial abundances are generally followed by a greater number of viral particles. The literature data were obtained from Barros et al. (2010)BARROS, N., FARJALLA, V.F., SOARES, M.C., MELO, R.C.N. and ROLAND, F. Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake. Applied and Environmental Microbiology, 2010, 76(21), 7194-7201. http://dx.doi.org/10.1128/AEM.01161-10. PMid:20833790.
http://dx.doi.org/10.1128/AEM.01161-10... (Amazon lakes), Almeida et al. (2015)ALMEIDA, R.M., ROLAND, F., CARDOSO, S.J., FARJALLA, V.F., BOZELLI, R.L. and BARROS, N.O. Viruses and bacteria in floodplain lakes along a major Amazon tributary respond to distance to the Amazon River. Frontiers in Microbiology, 2015, 6, 158. http://dx.doi.org/10.3389/fmicb.2015.00158. PMid:25788895.
http://dx.doi.org/10.3389/fmicb.2015.001... (Amazon lakes), Cabral et al. (2017)CABRAL, A.S., LESSA, M.M., JUNGER, P.C., THOMPSON, F.L. and PARANHOS, R. Virioplankton dynamics are related to eutrophication levels in a tropical urbanized bay. PLoS One, 2017., 12(3), e0174653. http://dx.doi.org/10.1371/journal.pone.0174653.
http://dx.doi.org/10.1371/journal.pone.0... (Guanabara Bay) and Junger et al. (2018)JUNGER, P.C., AMADO, A.M., PARANHOS, R., CABRAL, A.S., JACQUES, S.M.S. and FARJALLA, V.F. Salinity drives the virioplankton abundance but not production in tropical coastal lagoons. Microbial Ecology, 2018, 75(1), 52-63. http://dx.doi.org/10.1007/s00248-017-1038-3. PMid:28721503.
http://dx.doi.org/10.1007/s00248-017-103... (coastal lagoons in the state of Rio de Janeiro).

Figure 1 Viruses are extremely small (20-200 nm), smaller than bacterial cells (> 1000 nm), which in turn are smaller than animal and plant cells. nm = nanometer; μm = micrometer; cm = centimeter. Adapted from Melo (2018)MELO, R.C.N. Células & microscopia: princípios e práticas. 2. ed. Barueri: Manole, 2018, 300 p., with permission.

Figure 2 Simplified illustration of the three main virus replication strategies: lytic cycle, lysogenic cycle and chronic infection.

Figure 3 Image of an aquatic ecosystem bacterium infected with viruses, observed by transmission electron microscopy. The black “dots” indicate the presence of non-tailed bacteriophages in the bacterial cytoplasm. The boxed area shows a zoomed-in view of the structure of the viral protein capsule (capsid), composed of several repetitive morphological units (highlighted in blue). Image reproduced from Barros et al. (2010)BARROS, N., FARJALLA, V.F., SOARES, M.C., MELO, R.C.N. and ROLAND, F. Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake. Applied and Environmental Microbiology, 2010, 76(21), 7194-7201. http://dx.doi.org/10.1128/AEM.01161-10. PMid:20833790.
http://dx.doi.org/10.1128/AEM.01161-10... , with permission.

Figure 4 Illustration of the effects of the “viral loop” on aquatic food webs. Viruses (A) break host cells, which are often unicellular organisms such as bacteria (B) and phytoplankton (C), thereby releasing nutrients (carbon, nitrogen and phosphorus; CNP) into the water. In this way, viruses divert the amount of carbon that would reach higher trophic levels, such as microzooplankton (flagellates and ciliates - D), macrozooplankton (rotifers, cladocerans and copepods - E) and predators (e.g., fish - F), and release them back to the base of aquatic food webs (B and C). The black arrows indicate the regular flow of carbon in aquatic food webs, whereas the red arrows indicate the flows mediated by viruses. The width of the red arrows roughly represents the magnitude of these flows based on the relative abundance and biomass of these organisms usually found in aquatic ecosystems. Note that this is a theoretical picture and the width of the arrows may change between specific ecosystems. Figure adapted from Farjalla et al. (2011)FARJALLA, V.F., AMADO, A.M. and ESTEVES, F.A. Bacterioplâncton. In: F.A. ESTEVES, ed. Fundamentos de limnologia. 3. ed. Rio de Janeiro: Interciência, 2011, pp. 355-373..

Figure 5 Regression between viruses and bacterial counts from water samples collected in Brazilian aquatic ecosystems. The strong positive relationships (Amazon lakes: n = 66, r² = 0.84, p <0.01; Coastal lagoons: n = 18, r² = 0.39; p <0.01; Guanabara Bay: n = 246, r² = 0.53; p <0.01) indicate that high bacterial abundances are generally followed by a greater number of viral particles. The literature data were obtained from Barros et al. (2010)BARROS, N., FARJALLA, V.F., SOARES, M.C., MELO, R.C.N. and ROLAND, F. Virus-bacterium coupling driven by both turbidity and hydrodynamics in an Amazonian floodplain lake. Applied and Environmental Microbiology, 2010, 76(21), 7194-7201. http://dx.doi.org/10.1128/AEM.01161-10. PMid:20833790.
http://dx.doi.org/10.1128/AEM.01161-10... (Amazon lakes), Almeida et al. (2015)ALMEIDA, R.M., ROLAND, F., CARDOSO, S.J., FARJALLA, V.F., BOZELLI, R.L. and BARROS, N.O. Viruses and bacteria in floodplain lakes along a major Amazon tributary respond to distance to the Amazon River. Frontiers in Microbiology, 2015, 6, 158. http://dx.doi.org/10.3389/fmicb.2015.00158. PMid:25788895.
http://dx.doi.org/10.3389/fmicb.2015.001... (Amazon lakes), Cabral et al. (2017)CABRAL, A.S., LESSA, M.M., JUNGER, P.C., THOMPSON, F.L. and PARANHOS, R. Virioplankton dynamics are related to eutrophication levels in a tropical urbanized bay. PLoS One, 2017., 12(3), e0174653. http://dx.doi.org/10.1371/journal.pone.0174653.
http://dx.doi.org/10.1371/journal.pone.0... (Guanabara Bay) and Junger et al. (2018)JUNGER, P.C., AMADO, A.M., PARANHOS, R., CABRAL, A.S., JACQUES, S.M.S. and FARJALLA, V.F. Salinity drives the virioplankton abundance but not production in tropical coastal lagoons. Microbial Ecology, 2018, 75(1), 52-63. http://dx.doi.org/10.1007/s00248-017-1038-3. PMid:28721503.
http://dx.doi.org/10.1007/s00248-017-103... (coastal lagoons in the state of Rio de Janeiro).

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Not all viruses in nature are human enemies: a perspective on aquatic virus ecology in Brazil

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[1] *e-mail: pedro.junger@gmail.com