Uncoupled viral and bacterial distributions in coral reef waters of Tuamotu Archipelago (French Polynesia)
Highlights
► No correlation was observed between the distributions of bacteria and virus. ► The role of viruses in the coral reef ecosystems has yet to be studied. ► Fraction of visibly infected cells (FIC) by viruses was negligible.
Introduction
There is no doubt of the ecological importance of bacterioplankton in coral reef systems but the role of virioplankton in these ecosystems has, to our knowledge, yet to be studied. Viruses are the numerically dominant biological entities in the ocean and viral infection is a major structuring process in the dynamics of marine microbial communities (Fuhrman, 1999, Suttle, 2005). Viral lysis of autotrophic and heterotrophic microorganisms influences the rate of nutrient cycling through microbial food webs (Proctor and Fuhrman, 1990, Fuhrman, 1999). Recent studies of marine systems have shown that virus mediated mortality of bacterioplankton is greater in nutrient rich habitats where contact rates with potential hosts are high (Weinbauer, 2004).
Most virioplankton in the environment infect bacterioplankton (bacteriophages or, simply, phages) and, in general, the distributions of viral populations often mirror the bacterial distributions (Hewson et al., 2001, Middelboe et al., 2003). Variability amongst coral reef bacterial communities has been investigated at a variety of spatial and temporal scales (Moriarty, 1979, Moriarty et al., 1985, Paul et al., 1986, Hoppe et al., 1988, Gast et al., 1998) and significant variations in abundance, activity and composition have been observed over small spatial and temporal scales (Paul et al., 1986, Gast et al., 1998, van Duyl and Gast, 2001, Frias-Lopez et al., 2002, Rohwer et al., 2002). The role of virioplankton in coral reef systems remain relatively unexplored (Seymour et al., 2005, Mari et al., 2007, Dinsdale et al., 2008), as well as the presence and the roles of viruses associated with healthy and diseased corals which warrant further investigation (Weil et al., 2006, Patten et al., 2008). Nothing is known on the mode of viral infections and the life strategy of virioplankton in coral reef systems.
In addition to their role in the mortality of phyto-and bacterioplankton, viral lysis products (e.g., dissolved organic matter (DOM)) from cells through the viral shunt can be taken up by prokaryotes, thereby stimulating the growth of heterotrophic bacterioplankton (Wilhelm and Suttle, 1999, Thingstad, 2000). Tropical coral lagoon systems are also an interesting environment for the study of carbon cycling, as they are often characterized by low nutrient (DOM) and chlorophyll concentrations (Rochelle-Newall et al., 2008). The recycling of DOM by heterotrophic bacterioplankton is one of the major organic matter transformation pathways and could explain bacterial and viral distributions (Del Giorgio and Davies, 2003). Virioplankton are, therefore, believed to have a significant effect on aquatic environments.
French Polynesia is made up of several groups of islands in the South Pacific gyre with 84 atolls surrounded by oligotrophic waters. The lagoons are of great importance to the economy of French Polynesia, where farming of pearl oyster, Pinctada margaritifera, is the major source of export earnings (Andréfouët et al., 2012). Though originally benthic, P. margaritifera is now reared on suspended ropes and the resulting interactions with pelagic communities raise questions about the ability of planktonic food webs to sustain this increased animal production. In atoll lagoons, the primary production is mainly achieved by picophytoplankton (Charpy, 1996, Charpy and Blanchot, 1996), whereas the biomass is dominated by low-producing bacteria (Torréton and Dufour, 1996). As both picoplankters are in a size range unavailable to oysters (Pouvreau et al., 1999), phagotrophic protists may act as an intermediate between the dominant picoproduction and bivalves (Loret et al., 2000).
To determine the potential role of virioplankton in bacterioplankton dynamics in coral reef systems, the spatial distribution of virus-like particles (VLP) and bacterial communities was determined in the pelagic zone, as well as the dissolved organic carbon and the chlorophyll-a concentrations within two atoll lagoons in the Tuamotu Archipelago. The fraction of lysogenic bacterial cells (FLC) and the fraction of infected bacterial cells (FIC) were also determined to infer the prevalence of these two modes of infection. A broad study was made of the VLP and bacterial communities in the benthic zone where there is very little data on virioplankton dynamics at tropical latitudes, especially in coral reef systems.
Section snippets
Study sites and sampling
This study was conducted in two atolls (Ahe and Takaroa) located 500 km northeast of Tahiti in the north of the Tuamotu Archipelago between August 20 and 30, 2009 (Fig. 1; see details in Thomas et al., 2010). Ahe lagoon is 142 km2 in area with a maximum depth close to 70 m and can be defined as a semi-enclosed atoll. There is one deep passage to the ocean in the northwest and there are several reef-flats (inferior to 50 cm depth) along the reef rim. Four stations were sampled (A1, A3, A9, A11)
Physical and chemical conditions
The water temperature was comparable in the two atoll lagoons, with a mean of 27.2 °C. In the oceanic zone, values were not significantly different from those recorded in the atolls (26.8 ± 0.58 °C; Table 1). Chlorophyll-a concentrations were significantly different between the two atolls (p = 0.001), with higher values found for Ahe (0.32 ± 0.10 μg l−1). In oceanic zones, chlorophyll concentrations were significantly lower than those in the lagoons (0.13 ± 0.04 μg l−1; p = 0.003) (Table 1). Mean values of DOC
Discussion
Many studies have dealt with the viral compartment in tropical ecosystems (Seymour et al., 2005, Dinsdale et al., 2008, Weinbauer et al., 2010) by exploring the relationship between bacterial and viral distributions. This study provides new data on these two biological components in two coral reef systems, and especially on a variety of viral parameters. To the best of our knowledge, this study provided the first data on lytic and lysogenic strategies of phages in coral reef environments. Other
Acknowledgements
This work was supported by the European Development Fund, in collaboration with the Service de la Perliculture and the University of French Polynesia. We should like to thank P. Calquin and P. Bonin for their valuable help in collecting samples. Constructive comments and suggestions were provided by the reviewers.
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