Metatranscriptome Data Support the Existence of Two Distinct Morphotypes in a Single Parmalean Species in Natural Environments

Abstract

Parmales, the sister clade of diatoms, includes isolates exhibiting one of two morphotypes: a silicified non-flagellated form (S-type) and a naked flagellated form (F-type). Although the alternation of these forms for a single isolate has not been formally established, these morphotypes have been hypothesized to represent alternating stages of a single parmalean population. We herein investigated the global expression patterns of S- and F-type markers by integrating parmalean environmental genomes and metatranscriptomic data from Tara Oceans. We detected the expression of both S- and F-type marker genes from individual environmental genomes, providing the first metatranscriptomic evidence supporting the hypothesis of a life cycle involving two morphotypes. Furthermore, the expression of F-type markers showed a broad distribution across various environmental conditions, whereas that of S-type markers was more restricted and associated with specific environmental conditions. Based on these patterns, we propose a threshold-based model in which F-type-dominated populations persist under a wide range of conditions, from oligotrophic to eutrophic environments, and a morphological switch to the S-type is triggered in a minor subset of F-type populations once environmental conditions exceed a critical threshold for growth. This study provides insights into the evolutionary acquisition of a cell type specialized for photoautotrophy in the common ancestor of parmaleans and diatoms.