Biochemical adaptation of phytoplankton to salinity and nutrient gradients in a coastal solar saltern, Tunisia

Abstract

The distribution of protein and carbohydrate concentrations of the particulate matter (size fraction: 0.45–160 μm) was studied, from 22 January 2003 to 02 December 2003, in three ponds of increasing salinity in the Sfax solar saltern (Tunisia). The coupling of N/P: DIN (DIN = NO₂⁻ + NO₃⁻ + NH₄⁺) to DIP (DIP = PO₄³⁻) with P/C: protein/carbohydrates ratios along salinity gradient allowed the discrimination of three types of ecosystems. Pond A1 (mean salinity: 45.0 ± 5.4) having marine characteristics showed enhanced P/C ratios during a diatom bloom. N/P and P/C ratios were closely coupled throughout the sampling period, suggesting that the nutritional status is important in determining the seasonal change in the phytoplankton community in pond A1. In pond A16 (mean salinity: 78.7 ± 8.8), despite the high nitrate load, P/C ratios were overall lower than in pond A1. This may be explained by the fact that dinoflagellates, which were the most abundant phytoplankton in pond A16 might be strict heterotrophs and/or mixotrophs, and so they may have not contributed strongly to anabolic processes. Also, N/P and P/C ratios were uncoupled, suggesting that cells in pond A16 were stressed due to the increased salinity caused by water evaporation, and so cells synthesized reserve products such as carbohydrates. In pond M2 (mean salinity: 189.0 ± 13.8), P/C levels were higher than those recorded in either pond A1 or A16. N/P and P/C were more coupled than in pond A16. Species in the hypersaline pond seemed paradoxally less stressed than in pond A16, suggesting that salt-tolerant extremophile species overcome hypersaline constraints and react metabolically by synthesizing carbohydrates and proteins.

Introduction

Coastal solar salterns have been constructed in many areas worldwide, and consist of a series of interconnected ponds of increasing salt concentration, ranging from that of seawater to saturation in the crystallizing ponds to gain halite from seawater and magnesium-rich bittern brines. Despite salterns harbor diverse prokaryotic and eukaryotic organisms (Oren, 2002, Elloumi et al., 2006, Elloumi et al., 2008a), and members of such natural communities may have salt adaptations that are not reflected in cultured organisms (Sørensen et al., 2005), field investigations of the change in the particulate protein and carbohydrate concentrations along the salinity gradient are very scarce. For example, the halotolerant unicellular green alga Dunaliella salina not only can adapt to a large spectrum of salt concentrations by accumulating glycerol to provide osmotic balance, but also directs its metabolism towards the formation of specific proteins in relation with changes in medium salinity (see review by Oren, 2005). For decades, the biochemical composition of the particulate matter in aquatic environments has been demonstrated to be governed by factors such as, light, temperature, nutrients, water movements, and the growth rate of the organisms involved (Myklestad, 1974, Butterwick et al., 2005), both in marine and freshwater ecosystems (Aleya, 1991, Meiners et al., 2003). On the other hand, several findings have provided evidence that halophilic organisms have specific ecophysiological and biological characteristics (DaSarma and Arora, 2002, Elevi Bardavid and Oren, 2008). However the ecophysiological significance of the biochemical change in the particulate matter in ponds of increasing salt concentrations are scarce. The lipid and protein composition of halophilic Archaea and Bacteria (Litchfield et al., 2000, Oren and Mana, 2002), as well as phytoplankton assemblages (Ayadi et al., in press) and the anostracan brine shrimp Artemia salina (Moraiti-Ioannidou et al., 2007, Guermazi et al., 2008) have been shown to vary with increasing salt concentration. In this study we report on the biochemical composition of the particulate matter contained in the 0.45–160 μm size fraction in three ponds of increasing salinity of the Sfax saltern (Tunisia). We hypothesized that micro-organisms contained in this fraction should exhibit interspecific differences in their response to both the salinity gradient and nutrient availability, which affect their ecophysiological status expressed by their protein to carbohydrate ratio (Aleya, 1991).