Genomic Analysis of Picochlorum Species Reveals How Microalgae May Adapt to Variable Environments

Abstract

Understanding how microalgae adapt to rapidly changing environments is not only important to science but can help clarify the potential impact of climate change on the biology of primary producers. We sequenced and analyzed the nuclear genome of multiple Picochlorum isolates (Chlorophyta) to elucidate strategies of environmental adaptation. It was previously found that coordinated gene regulation is involved in adaptation to salinity stress, and here we show that gene gain and loss also play key roles in adaptation. We determined the extent of horizontal gene transfer (HGT) from prokaryotes and their role in the origin of novel functions in the Picochlorum clade. HGT is an ongoing and dynamic process in this algal clade with adaptation being driven by transfer, divergence, and loss. One HGT candidate that is differentially expressed under salinity stress is indolepyruvate decarboxylase that is involved in the production of a plant auxin that mediates bacteria-diatom symbiotic interactions. Large differences in levels of heterozygosity were found in diploid haplotypes among Picochlorum isolates. Biallelic divergence was pronounced in P. oklahomensis (salt plains environment) when compared with its closely related sister taxon Picochlorum SENEW3 (brackish water environment), suggesting a role of diverged alleles in response to environmental stress. Our results elucidate how microbial eukaryotes with limited gene inventories expand habitat range from mesophilic to halophilic through allelic diversity, and with minor but important contributions made by HGT. We also explore how the nature and quality of genome data may impact inference of nuclear ploidy.

The genomes of polyextremophilic cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions

“…In such environments, they can represent up to 90% of the total biomass, competing with specialized Bacteria and Archaea (Seckbach, 1972), although some Cyanidiales strains also occur in more temperate environments (Qiu et al, 2013; Gross et al, 2002; Ciniglia et al, 2004; Barcytė et al, 2018; Iovinella et al, 2018). The integration and maintenance of HGT-derived genes, in spite of strong selection for genome reduction in these taxa (Qiu et al, 2015) underlines the potential ecological importance of this process to niche specialization (Schönknecht et al, 2013; Qiu et al, 2013; Raymond and Kim, 2012; Bhattacharya et al, 2013; Foflonker et al, 2018; Schönknecht et al, 2014). For this reason, we chose the Cyanidiales as a model lineage for studying eukaryotic HGT.…”

Systems Biology of Cold Adaptation in the Polyextremophilic Red Alga Galdieria sulphuraria

“…Horizontal gene transfer has facilitated the niche adaptation of Galdieria and other microorganisms by providing adaptive advantages (Schonknecht et al, 2013; Schönknecht et al, 2014; Foflonker et al, 2018). Five of the total 54 HGT gene candidates in G. sulphuraria RT22 gained variants (Rossoni et al, 2019).…”

“…Microorganisms rapidly acclimate and subsequently adapt to environmental change (López-Rodas et al, 2009; Huertas et al, 2011; Romero-Lopez et al, 2012; Osundeko et al, 2014; Foflonker et al, 2018). These adaptations are driven by natural selection and involve quantitative changes in allele frequencies and phenotype within a short period of time, a phenomenon known as microevolution.…”

Global distribution of Trebouxiophyceae diversity explored by high‐throughput sequencing and phylogenetic approaches

“…). Genus Picochlorum (included within Nannochloris – Like; Table S1) well‐known for its tolerance towards large variations in salinity has been isolated accordingly from marine and brackish environments alike (Foflonker et al ., ). However, in our study, these organisms appeared only in MA samples, possibly; even if they tolerate freshwater, it is still unclear if they can form viable populations under low salinity conditions.…”