Chloroplast genome evolution and phylogeny of the early‐diverging charophycean green algae with a focus on the Klebsormidiophyceae and Streptofilum

Abstract

The Klebsormidiophyceae are a class of green microalgae observed globally in both freshwater and terrestrial habitats. Morphology‐based classification schemes of this class have been shown to be inadequate due to the simple morphology of these algae, the tendency of morphology to vary in culture versus field conditions, and rampant morphological homoplasy. Molecular studies revealing cryptic diversity have renewed interest in this group. We sequenced the complete chloroplast genomes of a broad series of taxa spanning the known taxonomic breadth of this class. We also sequenced the chloroplast genomes of three strains of Streptofilum, a recently discovered green algal lineage with close affinity to the Klebsormidiophyceae. Our results affirm the previously hypothesized polyphyly of the genus Klebsormidium as well as the polyphyly of the nominal species in this genus, K. flaccidum. Furthermore, plastome sequences strongly support the status of Streptofilum as a distinct, early‐diverging lineage of charophytic algae sister to a clade comprising Klebsormidiophyceae plus Phragmoplastophyta. We also uncovered major structural alterations in the chloroplast genomes of species in Klebsormidium that have broad implications regarding the underlying mechanisms of chloroplast genome evolution.

Investigating the Evolution of Green Algae with a Large Transcriptomic Dataset

“…Our analyses generally found streptophytes to form a pectinate tree with Mesostigma and Chlorokybus forming a monophyletic group. Klebsormidiophyceae are the next major group in our analyses, but Glass et al . (2023) found Interfilum to form a clade branching before the Klebsormidiophyceae.…”

“…2014; Graham 1993). Since then, separate phylogenetic analyses using a combination of plastid, mitochondrial, and nuclear genes have recovered support for each clade being the true sister taxon (Glass et al . 2023; Finet et al .…”

“…2005). Recent advances, including application of models for heterotachous sequence evolution, and increased breadth of taxon sampling, have provided valuable new insights into the diversification of Chloroplastida, but many unsolved problems remain (Glass et al . 2023; Del Cortona et al .…”

Phylogenomics definesStreptofilumas a novel deep branch of streptophyte algae

“…A phylogeny built from a combination of the nuclear 18S rRNA and the plastidial rbcL genes suggested that S. capillatum represents a deep separate streptophyte lineage, even possibly sister to all other streptophytes combined 1 . More recently, Glass et al 2 sequenced the plastid genome of S. capillatum and corroborated its separate phylogenetic status by analyzing a set of 44 plastid-encoded proteins, placing the alga with full support sister to nearly all other streptophytes combined except for the more basally positioned genera Mesostigma and Chlorokybus . From this perspective, the results of the phylotranscriptomic analysis reported by Bierenbroodspot et al 3 are highly surprising: having S. capillatum positioned within Klebsormidiophyceae in a tight clade together with representatives of the genus Interfilum (even making the genus paraphyletic), their tree separates the alga from the position implied by the plastid genes-based phylogeny by five fully supported nodes.…”

“…Their seemingly well-studied phylogenetic diversity was recently enriched by the discovery of Streptofilum capillaum , a simple filamentous alga forming a novel deep streptophyte lineage in a two-gene phylogeny 1 . A subsequent phylogenetic analysis of plastid genome-encoded proteins resolved Streptofilum as a sister group of nearly all known streptophytes, including Klebsormidiophyceae and Phragmoplastophyta (Charophyceae, Coleochaetophyceae, Zygnematophyceae, and embryophytes) 2 . In a stark contrast, another recent report, published in Current Biology by Bierenbroodspot et al 3 , presented a phylogenetic analysis of 845 nuclear loci resolving S. capillatum as a member of Klebsormidiophyceae, nested among species of the genus Interfilum .…”