Taxa novelty, resistance and resilience of halophilic microbial communities of solar salterns to environmental changes

Abstract

ReExtremely halophilic communities thriving in coastal solar salterns are principally influenced by two main environmental factors: high salt concentrations and high sunlight irradiation. In this thesis, we focused on the study of the microbial diversity and dynamics by means of culture-dependent (tandem approach using MALDI-TOF targeting whole cell biomass and 16S rRNA gene phylogenetic reconstruction of recovered isolates) and culture-independent (metagenomic data) methodologies. The culture-dependent approach was applied to the comparison of sediments and brines of eight geographically distinct sampling sites based on more than 4,200 isolates. Isolate characterization showed that we recovered members of four new genera and nine new species of the Halobacteria class, as well as representatives of the phylotype II of Salinibacter ruber (EHB-2) that had been refractory to isolation over the past fifteen years. Further, a new species of the Salinibacter genus which was classified as Salinibacter altiplanensis, was also recovered. The genome sequences of different species of the phylum Rhodothermaeota were sequenced and the genetic repertoire along an evolutionary gradient formed by these genome, focusing primarily on intraspecific variability. Analysis of members of the Salinibacter ruber phylotypes EHB-1 and EHB-2 revealed significant differences in several functional traits such as rhodopsin genes content, CRISPR-Cas systems and one T6SS secretion system that could give ecological advantages to the EHB-2 phylotypes and drive its speciation. The dynamics of these genomes as well as the remaining microbial community of salterns were also investigated, in situ, by controlled environmental perturbations related to light-intensity and salinity, in addition to the interaction between sediment and brines. We showed, by using a metagenomic approach, that light and salinity acted as deterministic factors that ultimately drove the establishment of recurrent microbial communities under near-saturation salt concentrations. Microbial communities adapted to high irradiation and salinity correlated with the known assemblages, were mainly dominated by Haloquadratum spp. and Salinibacter spp, which, generally, seemed to be highly resilient to environmentally driven changes in light intensity and salt concentrations. On the other hand, under low irradiation and salinity, different, less resistant and resilient communities established which were characterized by a higher diversity of photosynthetic and novel organisms. Stochastic processes were transiently significant during the transition phase conditions, albeit still limited when compared to deterministic processes, solely. Stochastic processes were largely associated with the activity of distinct primary producers, light and salt adaptation, and virus predation.