The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms

Abstract

Benthic diatoms are the main primary producers in shallow freshwater and coastal environments, fulfilling important ecological functions such as nutrient cycling and sediment stabilization. However, little is known about their evolutionary adaptations to these highly structured but heterogeneous environments. Here, we report a reference genome for the marine biofilm-forming diatom Seminavis robusta, showing that gene family expansions are responsible for a quarter of all 36,254 protein-coding genes. Tandem duplications play a key role in extending the repertoire of specific gene functions, including light and oxygen sensing, which are probably central for its adaptation to benthic habitats. Genes differentially expressed during interactions with bacteria are strongly conserved in other benthic diatoms while many species-specific genes are strongly upregulated during sexual reproduction. Combined with re-sequencing data from 48 strains, our results offer insights into the genetic diversity and gene functions in benthic diatoms.

Diurnal transcript profiling of the diatomSeminavis robustareveals adaptations to a benthic lifestyle

“…Most rhythmic protein-coding genes displayed a 24-h (92.5%) or 12-h (7.5%) periodicity, and similar to reports in other diatoms, were predominantly phasing at dusk and at night ( Figure 1C, Supplemental Data Set 2) (Smith et al, 2016;Ashworth et al, 2013;Goldman et al, 2019). We cross-referenced the 10,145 protein-coding genes that were not expressed during the diurnal cycle in a publicly available S. robusta expression atlas that reports on transcriptional activity during sexual reproduction, abiotic stress and diatom-bacterial interactions (Osuna-Cruz et al, 2020). More than half (5,315) of non-diurnal genes were transcriptionally active in at least one condition, although at lower expression levels than diurnally expressed genes (Supplemental Figure 4A).…”

“…Evolutionary analysis of rhythmic genes points towards ancient daytime functions and diatom-specific expression at night Phylostratigraphic analysis, which explores protein homology in a wide set of species to date the origin of specific genes, revealed that rhythmic protein-coding genes were enriched in eukaryote and stramenopile age, while non-significantly rhythmic genes displayed enrichment in species-specific genes (Figure 2A). The latter group of genes was mainly enriched in genes upregulated under different stress conditions in the S. robusta expression atlas (Osuna-Cruz et al, 2020), while the set of rhythmic genes was predominantly enriched in downregulated genes under these conditions ( Figure 2B). These results suggest that while phylogenetically old rhythmic genes play a role in basal diurnal functions, young and non-rhythmic genes are more important in specific environmental contexts that are not part of the diurnal regime, a trend also observed in land plants and several microalgae (Ferrari et al, 2019).…”

“…We observed a peak at night for three casein kinase 1 (CK1) homologs while the blue-light sensing cryptochrome/photolyase family 1 (CPF1) gene was peaking at dawn, analogous to P. tricornutum and N. oceanica (Poliner et al, 2015). Genes encoding G-protein-coupled receptor (GPCR) rhodopsin-like proteins, which are prominently expanded in the S. robusta genome and conserved in several other benthic diatoms, were predominantly expressed at dusk and at night (Supplemental Figure 18) (Osuna-Cruz et al, 2020). Given the sensitivity of animal rhodopsins to extremely low levels of light, they may be involved in photoreception inside sediments or phototrophic biofilms which exhibit strong light attenuation on a millimeter scale (Reingruber et al, 2015;Congestri and Albertano, 2011;MacIntyre et al, 1996).…”

“…The quality of adaptor-trimmed reads belonging to 161 samples from the previously published S. robusta gene expression atlas (Osuna-Cruz et al, 2020) and the 36 new diel cycle samples was assessed using FastQC v0.11.4 (Andrews, 2010). All reads were mapped to the S. robusta genome using STAR v2.5.2 (--sjdbGTFfeatureExon, --alignIntronMax 6000) (Dobin et al, 2013;Osuna-Cruz et al, 2020) followed by the removal of chimeric alignments and retention of uniquely mapping reads using samtools v1.3 (-F 4 -q 1) (Li et al, 2009). Next, these alignments were split per scaffold and genome-guided Trinity De novo Transcriptome v2.6.6 was executed (--genome_guided_bam, --genome_guided_max_intron 6000) (Grabherr et al, 2011), generating 221,735 transcripts.…”

Light Regulation of LHCX Genes in the Benthic Diatom Seminavis robusta

“…The expansion of gene families seems to be a general feature of S. robusta and is not exclusive to the LHCX genes. The large genome size of S. robusta allows for duplication events which could in turn lead to adaptive evolution (Osuna-Cruz et al, 2020). A large set of LHCX genes could be required to cope with highly variable light conditions.…”