Life cycle and functional genomics of the unicellular red alga Galdieria for elucidating algal and plant evolution and industrial use

Abstract

Sexual reproduction is widespread in eukaryotes; however, only asexual reproduction has been observed in unicellular red algae, including Galdieria , which branched early in Archaeplastida. Galdieria possesses a small genome; it is polyextremophile, grows either photoautotrophically, mixotrophically, or heterotrophically, and is being developed as an industrial source of vitamins and pigments because of its high biomass productivity. Here, we show that Galdieria exhibits a sexual life cycle, alternating between cell-walled diploid and cell wall–less haploid, and that both phases can proliferate asexually. The haploid can move over surfaces and undergo self-diploidization or generate heterozygous diploids through mating. Further, we prepared the whole genome and a comparative transcriptome dataset between the diploid and haploid and developed genetic tools for the stable gene expression, gene disruption, and selectable marker recycling system using the cell wall–less haploid. The BELL/KNOX and MADS-box transcription factors, which function in haploid-to-diploid transition and development in plants, are specifically expressed in the haploid and diploid, respectively, and are involved in the haploid-to-diploid transition in Galdieria , providing information on the missing link of the sexual life cycle evolution in Archaeplastida. Four actin genes are differently involved in motility of the haploid and cytokinesis in the diploid, both of which are myosin independent and likely reflect ancestral roles of actin. We have also generated photosynthesis-deficient mutants, such as blue-colored cells, which were depleted in chlorophyll and carotenoids, for industrial pigment production. These features of Galdieria facilitate the understanding of the evolution of algae and plants and the industrial use of microalgae.

Deep evolution of MADS-box genes in Archaeplastida

“…Deletion of the only MADS-box gene of Galdiera sp. prevents these red algae from progressing from gametophyte to sporophyte (Hirooka, et al 2022) while overexpression of the MADS-box gene of the chlorophyte green algae Coccomyxa subellipsoidea leads to formation of polyploid multinucleate cells (Nayar and Thangavel 2021). Based on this very limited functional data, one may hypothesize that MADS-domain proteins in archaeplastid algae are involved in basic cell-biological processes like cell-cycle progression as has been observed for some MADS-box genes in animals and fungi (Elble and Tye 1992; Badodi, et al 2015) or basic cell-differentiation processes as in amoeba and animals (Galardi-Castilla, et al 2013; Wang, et al 2018).…”

“…Only one MADS-box gene has been identified in the red alga Cyanidioschyzon merolae (Stiller, et al 2012) and in Galdiera sp. (Hirooka, et al 2022). In Galdiera sp.…”

“…the MADS-box gene is specifically expressed in the sporophyte and has been hypothesized to be involved in the transition from gametophyte to sporophyte. All of these MADS-box genes from red algae are proposed to be Type II but no K box was reported (Stiller, et al 2012; Hirooka, et al 2022).…”

Discovery of sex in an extremophilic red alga

“…Were I still teaching upper-level biology courses, I would for sure assign the reading and discussion of Hirooka et al., “Life Cycle and Functional Genomics of the Unicellular Red Alga Galdieria for Elucidating Algal and Plant Evolution and Industrial Use” ( 1 ). It tells the engrossing tale of an unexpected discovery and the exploration of its important ramifications in both basic and applied bioscience, with a clear plot line, excellent data, and high-quality graphics.…”

“…1 of ref. 1 ). It can supplement photosynthesis with more than 50 different carbon sources, including organic materials present in wastewater, and it can grow in the dark to high densities in laboratory bioreactors when these supplements are provided ( 5 ).…”