Molecular physiology of Antarctic diatom natural assemblages reveals multiple strategies contributing to their ecological success

Abstract

The continental shelf of the Western Antarctic Peninsula (WAP) is a highly variable system characterized by strong cross-shelf gradients, rapid regional change and large blooms of phytoplankton, notably diatoms. Rapid environmental changes coincide with shifts in plankton community composition and productivity, food web dynamics and biogeochemistry. Despite progress in identifying important environmental factors influencing plankton community composition in the WAP, the molecular basis for their survival in this oceanic region, as well as variations in species abundance, metabolism and distribution remain largely unresolved. Across a gradient of physicochemical parameters, we analyzed the metabolic profiles of phytoplankton as assessed through metatranscriptomic sequencing. Distinct phytoplankton communities and metabolisms closely mirrored the strong gradients in oceanographic parameters that existed from coastal to offshore regions. Diatoms were abundant in coastal, southern regions, where colder and fresher waters were conducive to a bloom of the centric diatom, Actinocyclus. Members of this genus invested heavily in growth and energy production; carbohydrate, amino acid and nucleotide biosynthesis pathways; and coping with oxidative stress, resulting in uniquely expressed metabolic profiles compared to other diatoms. We observed strong molecular evidence for iron limitation in shelf and slope regions of the WAP, where diatoms in these regions employed iron-starved induced proteins, a geranylgeranyl reductase, aquaporins, and urease, among other strategies, while limiting the use of iron-containing proteins. The metatranscriptomic survey performed here revealed functional differences in diatom communities and provides further insight into the environmental factors influencing the growth of diatoms and their predicted response to changes in ocean conditions.

Widespread use of proton-pumping rhodopsin in Antarctic phytoplankton

“…Sequences were quality filtered with Trimmomatic v0.38 and assembled as described in ref. 55 . A consensus assembly was representative of all expressed genes of the microeukaryote community along the WAP and was used in the subsequent annotation and read count steps.…”

“…For functional annotations, consensus sequences were searched against the Kyoto Encyclopedia of Genes and Genomes (KEGG) database v2018 by similarly using Diamond BLASTX and a 10 −5 e-value. Because KEGG only provides KOs for functionally annotated genes, KEGG gene definitions for iron-starvation-induced proteins ( ISIP s) and RHO sequences were manually performed ( 55 ). Taxonomic annotations of RHO and ISIP3 were assigned using Diamond BLASTX v2.0.4 based on homology (e-value cutoff of 10 −5 ) to PhyloDB v1.075, a custom database curated by the Allen Lab (Scripps Oceanographic Institute), consisting of eukaryotic genomes and the transcriptomes from the Marine Microbial Eukaryote Transcriptome Sequencing Project.…”