Research Article: Virioplankton dynamics are related to eutrophication levels in a tropical urbanized bay

Date Published: March 31, 2017

Publisher: Public Library of Science

Author(s): Anderson S. Cabral, Mariana M. Lessa, Pedro C. Junger, Fabiano L. Thompson, Rodolfo Paranhos, Jiang-Shiou Hwang.


Virioplankton are an important and abundant biological component of marine and freshwater ecosystems. Often overlooked, aquatic viruses play an important role in biogeochemical cycles on a global scale, infecting both autotrophic and heterotrophic microbes. Viral diversity, abundance, and viral interactions at different trophic levels in aqueous environments are not well understood. Tropical ecosystems are less frequently studied than temperate ecosystems, but could provide new insights into how physical and chemical variability can shape or force microbial community changes. In this study, we found high viral abundance values in Guanabara Bay relative to other estuaries around the world. Viral abundance was positively correlated with bacterioplankton abundance and chlorophyll a concentrations. Moreover, prokaryotic and viral abundance were positively correlated with eutrophication, especially in surface waters. These results provide novel baseline data on the quantitative distribution of aquatic viruses in tropical estuaries. They also provide new information on a complex and dynamic relationship in which environmental factors influence the abundance of bacterial hosts and consequently their viruses. Guanabara Bay is characterized by spatial and seasonal variations, and the eutrophication process is the most important factor explaining the structuring of virioplankton abundance and distribution in this tropical urbanized bay.

Partial Text

Viruses are the most abundant biological entities on the planet [1–3] and are found in both marine and freshwater ecosystems [4], in and on sediments, in surface waters, and in deep seas [5]. It is currently estimated that global viral abundance (VA) may be as high as 1031 particles [5–7] and that viral activity significantly influences ecosystem structuring [8]. Viral lysis affects the composition and diversity of the microbial communities, suggesting that virioplankton are an important component of the microbial food web [7,9–11]. Nutrients are released during viral lysis and thus redistributed into the water column. The consequent transfer of microbial biomass influences nutrient cycling and alters pathways of organic carbon use by prokaryotes [11] in both natural and anthropogenic environments.

VA recorded in the study area ranged from 0.64 × 107 to 48.18 × 107 viruses mL-1. The highest counts were observed at the surface, while the lowest were found in bottom waters (Fig 2A and 2B; Table 1). It was possible to differentiate four different virus groups via flow cytometry (Fig 3A and 3B), as previously described [3,8,41]. They were termed V1, V2, V3, and V4, and were differentiated by their specific increase in fluorescence intensity. Groups V1, V2, and V3 represented, on average, 54%, 32%, and 14% of total VA, respectively. The most abundant group at all depths and sites was V1, which was also the group with the smallest particle sizes (Table 1). All groups exhibited a spatial gradient, with abundance highest in the BG-PQ region (inner bay) and decreasing towards the bay entrance (Fig 2A and 2B; Table 1). Group V4 abundances ranged from undetectable to 0.39 × 107 viruses mL-1. This group was mostly observed in surface waters from the innermost site (BG-PQ), although its abundance was generally very low and represented no more than 2% of total VA at this site.

In this study, the VA values observed in GB were among the highest reported for estuarine waters (Table 5). Such VA counts are equivalent to Chesapeake and Moreton bays, and higher than those reported for the Yangtze River, Tampa Bay, and the Charente and Bach Dang estuaries. VA data from the global dataset cited indicate that estuaries are favorable environments for high VA, and that these high counts can be attributed to eutrophication and microbial activity in these environments.

This is the first report on viral abundance in GB (Rio de Janeiro, Brazil), where VA counts are among the highest reported globally. A longer time series could confirm the seasonal patterns observed during the present study; however, our three-year data series suggests that VA in the bay is characterized by spatial and seasonal variations related to environmental conditions and anthropogenic impacts. High correlations between the abundance of viruses and their primary hosts (bacteria) in surface waters, suggests that the high eutrophication in GB is the main driver structuring microbial communities. This study thus provides further indication that eutrophication is a key factor in microbial structuring in tropical estuaries.




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