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Volvox sect. Volvox is a group of green algae with unique morphological features (thick cytoplasmic bridges between somatic cells and spiny zygote walls) and a worldwide distribution. Despite research interest in the diversity of organisms in ancient lakes, Volvox sect. Volvox from ancient lakes worldwide has not been identified to the species level. Here, we established clonal cultures of two species of this group originating from Lake Biwa, an ancient lake in Japan, and performed identification based on morphological and molecular data. One was identified as Volvox kirkiorum based on the nuclear ribosomal DNA internal spacer region (ITS) sequence, bisexual (monoicous or monoecious) spheroids, and zygote morphology. The other showed genetic separation from related species based on the secondary structure of the ITS and results of phylogenetic analysis of a combined data set from the nuclear actin gene, ITS, and two plastid genes (large subunit of RuBisCO and photosystem II CP43 apoprotein gene); it represented a new phylogenetic lineage within Volvox sect. Volvox, suggesting possible endemism in Lake Biwa. This species produced bisexual spheroids with different zygote morphology and zygote number from other species with bisexual spheroids in Volvox sect. Volvox. Therefore, Volvox biwakoensis Nozaki et H. Yamaguchi sp. nov. is described herein. This is the first endemic species of the genus Volvox described from an ancient lake., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Nozaki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Volvox sect. Volvox is an interesting group of green algae; it comprises mostly monoicous species, but evidence suggests an evolution towards dioicy. Based on cultured strains originating from Thailand, we describe Volvox longispiniferus, a novel species in Volvox sect. Volvox. This species is distinguished from others in the section by the large number of sperm packets in its monoicous sexual spheroids and by the long spines on its zygote wall. Phylogenetic analyses indicate that V. longispiniferus is distinct from the other species of two monophyletic groups within Volvox sect. Volvox. In addition, the novel species produces more zygotes when different cultures are combined compared with a single culture, suggesting a preference for outcrossing., Competing Interests: The authors have declared that no competing interests exist.

Volvox rousseletii is a dioecious species belonging to Volvox sect. Volvox that has previously only been found in Africa. During field surveys in a large dam lake (Lake Sagami) in Kanagawa Prefecture, central Japan, we encountered a Volvox sect. Volvox species that produces dioecious sexual spheroids in the water column. Although sexual induction of this species in culture did not produce adequately well-developed sexual spheroids for species identification, molecular data directly obtained from field-collected sexual spheroids verified the identity of field-collected male and female sexual spheroids as well as cultured materials. Based on molecular and morphological data, the species was identified as V. rousseletii. This is the first record of a dioecious species of Volvox sect. Volvox in Japan., Competing Interests: The authors have declared that no competing interests exist.

Volvox is a very interesting oogamous organism that exhibits various types of sexuality and/or sexual spheroids depending upon species or strains. However, molecular bases of such sexual reproduction characteristics have not been studied in this genus. In the model species V. carteri, an ortholog of the minus mating type-determining or minus dominance gene (MID) of isogamous Chlamydomonas reinhardtii is male-specific and determines the sperm formation. Male and female genders are genetically determined (heterothallism) in V. carteri, whereas in several other species of Volvox both male and female gametes (sperm and eggs) are formed within the same clonal culture (homothallism). To resolve the molecular basis of the evolution of Volvox species with monoecious spheroids, we here describe a MID ortholog in the homothallic species V. africanus that produces both monoecious and male spheroids within a single clonal culture. Comparison of synonymous and nonsynonymous nucleotide substitutions in MID genes between V. africanus and heterothallic volvocacean species suggests that the MID gene of V. africanus evolved under the same degree of functional constraint as those of the heterothallic species. Based on semi quantitative reverse transcription polymerase chain reaction analyses using the asexual, male and monoecious spheroids isolated from a sexually induced V. africanus culture, the MID mRNA level was significantly upregulated in the male spheroids, but suppressed in the monoecious spheroids. These results suggest that the monoecious spheroid-specific down regulation of gene expression of the MID homolog correlates with the formation of both eggs and sperm in the same spheroid in V. africanus.

The volvocine algae represent an excellent model lineage in which to study evolution of female and male genders based on comparative analyses of related species. Among these species, Volvox carteri has been extensively studied as a model of an oogamous and complex organism. However, it may have unique derived features that are not present in other species of Volvox. Therefore, information regarding the characteristics of sexual reproduction of other species of Volvox is also important. In 1971, Starr studied four types of sexuality in several global strains identified as Volvox africanus; however, further taxonomic studies of these strains have been lacking, and strains of three of the four sexual types are not available. Here, we studied the morphology, sexual reproduction, and taxonomy of two V. africanus-like species isolated recently from Lake Biwa, Japan. These two species were very similar to two sexual types described by Starr in 1971: one producing dioecious sexual spheroids in heterothallic strains and the other forming both male spheroids and monoecious spheroids in a single strain. The former species produced zygotes with a reticulate cell wall, whereas a smooth zygote wall was observed in the latter species as in V. africanus previously reported from various localities around the world. Our multigene phylogenetic analysis demonstrated that these are sister species to each other. However, the presence of a compensatory base change in the most conserved region of the secondary structure of nuclear ribosomal DNA internal transcribed spacer-2, hybrid inviability demonstrated by intercrossing experiments, and morphological differences in the density of abutment between the gelatinous material of adjacent cells (individual sheaths) in the spheroid supported the recognition of the two species, V. africanus having a smooth zygote wall and V. reticuliferus Nozaki sp. nov. having a reticulate zygote wall.

Volvocalean green algae have among the most diverse mitochondrial and plastid DNAs (mtDNAs and ptDNAs) from the eukaryotic domain. However, nearly all of the organelle genome data from this group are restricted to unicellular species, like Chlamydomonas reinhardtii, and presently only one multicellular species, the ∼4,000-celled Volvox carteri, has had its organelle DNAs sequenced. The V. carteri organelle genomes are repeat rich, and the ptDNA is the largest plastome ever sequenced. Here, we present the complete mtDNA and ptDNA of the colonial volvocalean Gonium pectorale, which is comprised of ∼16 cells and occupies a phylogenetic position closer to that of V. carteri than C. reinhardtii within the volvocine line. The mtDNA and ptDNA of G. pectorale are circular-mapping AT-rich molecules with respective lengths and coding densities of 16 and 222.6 kilobases and 73 and 44%. They share some features with the organelle DNAs of V. carteri, including palindromic repeats within the plastid compartment, but show more similarities with those of C. reinhardtii, such as a compact mtDNA architecture and relatively low organelle DNA intron contents. Overall, the G. pectorale organelle genomes raise several interesting questions about the origin of linear mitochondrial chromosomes within the Volvocales and the relationship between multicellularity and organelle genome expansion.