Elsevier

Estuarine, Coastal and Shelf Science

Volume 133, 20 November 2013, Pages 58-66
Estuarine, Coastal and Shelf Science

Freshwater prokaryote and virus communities can adapt to a controlled increase in salinity through changes in their structure and interactions

https://doi.org/10.1016/j.ecss.2013.08.013Get rights and content

Abstract

Little information exists on the ecological adaptive responses of riverine microorganisms to the salinity changes that typically occur in transitional waters. This study examined the precise effects of a gradual increase in salinity (+3 units per day for 12 days) on freshwater virus and prokaryote communities collected in the Red River Delta (northern Vietnam). The abundance, activity, morphology and diversity of both communities were examined along this simulated salinity gradient (0–36). Three main successive ecological stages were observed: (1) a continuous decline in prokaryotic and viral abundance from the start of the salinization process up to salinity 12–15 together with a strong decrease in the proportion of active cells, (2) a shift in both community compositions (salinity 9–15) and (3) a marked prevalence of lysogenic over lytic cycles up to salinity 21 followed by a collapse of both types of viral infection. Finally, after salinity 21, and up to seawater salinities (i.e. 36) the prokaryotic community showed multiple signs of recovery with their abundance and function even reaching initial levels. These results suggest that most of the physiological and phylogenetic changes that occurred within the salinity range 10–20 seemed to favor the installation of osmotically adapted prokaryotes accompanied by a specific cortege of viral parasites which might both be able to survive and even proliferate in saltwater conditions.

Introduction

Planktonic viruses form a ubiquitous and dynamic compartment, which is of primary ecological importance in aquatic environments (Weinbauer, 2004, Suttle, 2005). Although there is no doubt that prokaryotes are the main hosts for planktonic viruses (Fuhrman, 1999, Suttle, 2007), the role of environmental factors (nutrients, temperature, oxygen, light, organic and inorganic particles, etc.) in controlling virus–prokaryote interactions is still not clearly understood (Wilhelm et al., 2003, Weinbauer et al., 2009). Of these factors, least attention has probably been paid to salinity although it has been recognized as one of the most important factors determining the structure of the prokaryote community composition worldwide (Bouvier and del Giorgio, 2002, Crump et al., 2004, Hewson and Fuhrman, 2004, Lozupone and Knight, 2007). Information on the influence of salt on the relationships between prokaryotes and their viral parasites is very scarce even though this is crucial for understanding the role of planktonic phages in aquatic habitats.

Some studies have been carried out on natural salinity gradients in estuaries (Hewson et al., 2001, Auguet et al., 2005, Bettarel et al., 2011a), coastal lagoons (Schapira et al., 2009) and solar salterns (Guixa-Boixareu et al., 1996). However, these in situ studies only depict an instantaneous spatial pattern. Moreover, the effect of salinity alone is difficult to be determined in situ as interactions are also influenced by changes in other environmental parameters such as temperature, light, nutrients and predation. There is, therefore, a lack of information on the changes in a given assemblage subject to fluctuations in salinity alone. Preliminary attempts to evaluate the response of freshwater viruses and prokaryotes to simulated salinity shifts revealed that both communities declined sharply immediately after the addition of seawater (Cissoko et al., 2008, Bonilla-Findji et al., 2009). However, the sudden addition of salt in these experiments (freshwater taken directly to salinity 12 and 24) did not enable a close study of the successive ecological responses of prokaryotes and viruses and their ability to adapt over a more gradual increase in salinity.

To better understand the mechanisms that typically occur in estuaries or during the continuous salinization of groundwater, slow salinization rates are considered more appropriate as the mixing time between riverine and marine waters ranges over timescales from hours to days in many estuarine systems (Crump et al., 1999, Troussellier et al., 2002). This study mimicked the increase in salinity faced by freshwater prokaryotes and viruses during their descent to the sea and evaluated their potential for surviving and proliferating in seawater. The first aim was to study the changes in numbers, physiology and structure in the freshwater prokaryote communities subjected to progressively increasing salinity. The second aim was to assess whether such shifts were also accompanied by changes in the relationship between the freshwater prokaryote communities and their viral parasites. Salt was added gradually (increasing the salinity by 1.5 every 12 h) to 20-L microcosms over a 12 day period, until salinity reached the seawater level of 36. The study used freshwater collected from the tropical Red River Estuary (northern Vietnam).

Section snippets

Study site and experimental design

Freshwater samples were collected on March 10, 2009 in the Gia River (20°N, 106°E), a tributary of the Red River in Northern Vietnam (see map in Bettarel et al., 2011a). Three Nalgene polycarbonate bottles of 20-L were filled with sub-surface water (0.5 m depth) using a Niskin bottle. Two of these bottles, called salinized (SA) microcosms, were used as duplicates for salinization experiments and the third (to which nothing was added) served as control (C) to take account of the temporal and

Physico-chemical variables

Water temperature remained relatively stable (between 23 and 25 °C, data not shown) in all microcosms. Salinity had a very small but detectable effect on the DOC concentration with negative values of SaltEDOC along most of the salinity gradient (Fig. 1). This was particularly marked after the salinity 9 where concentrations in the salinized water and control water started to differ from each other.

Prokaryotes

Before the addition of salt, prokaryotic abundance at T0 was 4.9 × 106 cells mL−1. The SaltEprok

Discussion

Although the gradual addition of salt clearly resulted in a decrease of prokaryotic abundance until salinity 33, it did not lead to the total extinction of the community. On the contrary, the community showed signs of recovery after salinity 20, and a substantial regrowth up to typical seawater salinities (i.e. 36). This suggests that a fraction of the riverine prokaryote population is probably euryhaline and can maintain and even expand in oceanic waters (Rappé et al., 2000, Sleator and Hill,

Acknowledgments

This work was cofinanced by the EC2CO/PNEC project “HAIPHONG”, and grants from the French Institute of Research for Development (IRD) and the Vietnam Academy of Science and Technology (VAST).

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