Adaptive thermostability of light-harvesting complexes in marine picocyanobacteria

The ISME Journal (2017) 11, 112–124 © 2017 International Society for Microbial Ecology All rights reserved 1751-7362/17 www.nature.com/ismej ORIGINAL ARTICLE Adaptive thermostability of light-harvesting complexes in marine picocyanobacteria Justine Pittera1,2, Frédéric Partensky1,2 and Christophe Six1,2 1 Sorbonne Universités, Université Pierre and Marie Curie (Paris 06), UMR 7144, Marine Phototrophic Prokaryotes (MaPP) Team, Roscoff Cedex 29688, France and 2Centre National de la Recherche Scientifique, UMR 7144, Marine Plankton Group, Station Biologique, Roscoff Cedex, France Marine Synechococcus play a key role in global oceanic primary productivity. Their wide latitudinal distribution has been attributed to the occurrence of lineages adapted to distinct thermal niches, but the physiological and molecular bases of this ecotypic differentiation remain largely unknown. By comparing six strains isolated from different latitudes, we showed that the thermostability of their light-harvesting complexes, called phycobilisomes (PBS), varied according to the average sea surface temperature at strain isolation site. Comparative analyses of thermal unfolding curves of the three phycobiliproteins (PBP) constituting PBS rods suggested that the differences in thermostability observed on whole PBSs relied on the distinct molecular flexibility and stability of their individual components. Phycocyanin was the least thermostable of all rod PBP, constituting a fragility point of the PBS under heat stress. Amino-acid composition analyses and structural homology modeling notably revealed the occurrence of two amino-acid substitutions, which might have a role in the observed differential thermotolerance of this phycobiliprotein among temperature ecotypes. We hypothesize that marine Synechococcus ancestors occurred first in warm niches and that during the colonization of cold, high latitude thermal niches, their descendants have increased the molecular flexibility of PBP to maintain optimal light absorption capacities, this phenomenon likely resulting in a decreased stability of these proteins. This apparent thermoadaptability of marine Synechococcus has most probably contributed to the remarkable ubiquity of these picocyanobacteria in the ocean. The ISME Journal (2017) 11, 112–124; doi:10.1038/ismej.2016.102; published online 26 July 2016 Introduction Temperature is an environmental factor that greatly impacts the distribution of living forms on our planet. Temperature varies widely over the course of the day, seasons as well as across latitudes and therefore constitutes a major ecological constraint on the physiology of organisms and hence on the functioning of ecosystems. In particular, temperature is one of the main factors controlling inorganic carbon fixation, a process which in the oceans is prevalently ensured by phytoplanktonic cells (Falkowski, 1994; Behrenfeld et al., 2006). Among these, Prochlorococcus and Synechococcus, two highly abundant picocyanobacteria (o2 μm), are thought to be responsible for up to 25% of the global net oceanic primary production (Partensky et al., 1999; Flombaum et al., 2013). Whereas Prochlorococcus is restricted to the 40 °S–45 °N latitudinal band, Synechococcus occurs from the equator to polar circles (Neuer, 1992; Zwirglmaier et al., 2008; Correspondence: C Six, UMR 7144 UPMC-CNRS, Station Biologique de Roscoff, CS 90074, 29688 Roscoff, France. E-mail: Received 21 December 2015; revised 21 April 2016; accepted 24 April 2016; published online 26 July 2016 Huang et al., 2012), suggesting that this ubiquitous picocyanobacterium has developed efficient adaptive strategies to cope with natural temperature variations (Mackey et al., 2013; Pittera et al., 2014). Phylogenetic studies using various markers have evidenced the large genetic microdiversity occurring within the Synechococcus genus (Fuller et al., 2003; Ahlgren and Rocap, 2012). For instance, based on the high-resolution petB marker, ~ 15 clades and 28 subclades (Mazard et al., 2012) have been delineated within the main radiation, called subcluster 5.1 (Herdman et al., 2001). Basin-scale phylogeographical studies have shown that the most prevalent marine Synechococcus lineages, that is, clades I–IV, occupy distinct ecological niches (Zwirglmaier et al., 2008; Sohm et al., 2015). Clades I and IV are confined to nutrient-rich, cold or temperate waters at high latitude (430°N/S), whereas clades II and III preferentially thrive in warm waters, with the former being prevalent in subtropical and tropical open ocean and the latter dominating in the eastern Mediterranean Sea (Mella-Flores et al., 2011; Sohm et al., 2015; Farrant et al., 2016). Pittera et al. (2014) have evidenced a correspondence between the thermophysiology of Synechococcus clades I and II and their respective thermal niches. Indeed, members of these lineages were Phycobilisome thermoadaptation in Synechococcus J Pittera et al 113 shown to exhibit thermal preferenda (that is, temperature growth ranges and growth maxima) consistent with the seawater temperature at their isolation site, as well as a differential sensitivity to thermal stress. These genetically defined lineages, physiologically adapted to specific thermal niches, therefore correspond to different ‘temperature ecotypes’ (or ‘thermotypes’), a concept previously defined for Prochlorococcus clades HLI and HLII, which preferentially thrive in cool temperate waters and warm subtropical waters, respectively, a discrepancy also explained by the distinct growth temperature characteristics of representative isolates (Johnson et al., 2006; Zinser et al., 2007). Although other factors such as the macronutrients can be important sources of diversification within the marine Synechococcus radiation, recent field studies have demonstrated that temperature is one of the main factors explaining the variability of the genotypic composition of marine Synechococcus assemblages, with different thermotypes forming well-defined populations in distinct latitudinal bands at oceanic basin scales (Sohm et al., 2015; Farrant et al., 2016). Pittera et al. (2014) also showed that during thermal stress experiments the capacity of the temperature ecotypes to acclimate and endure temperature variations notably relies on their ability to optimize the functionality of their photosystem II (PS-II) at different temperatures. This macromolecular complex is indeed known to be a particularly temperature responsive component of the photosynthetic machinery (Murata et al., 2007). Like in red algae, the major PS-II light-harvesting antenna of Synechococcus is a giant, water soluble pigmentprotein complex, the phycobilisome (PBS). This macrocomplex, composed of a central core surrounded by six rods, is made of phycobiliproteins (PBP), themselves composed of two subunits (α and β) aggregated as hexameric discs (αβ)6. Different openchain tetrapyrrolic chromophores, the phycobilins, are bound to the apoprote (...truncated)