Mitochondrial genome structure, phylogenetic analyses and substitution rate estimation of the Oedogoniales

Abstract

The order Oedogoniales comprises three genera, Oedogonium, Oedocladium and Bulbochaete, which were classified based on traditional morphological criteria, and includes more than 600 described species. This group is economically important in astaxanthin production and the energy sector. However, only one mitochondrial genome (mitogenome) has been reported so far. This study determined the mitochondrial genomes of seven Oedogoniales species, including six Oedogonium species and Oedocladium prescottii. Comparative analyses between the newly determined mitogenomes and the previously reported Bulbochaete rectangularis var. hiloensis mitogenome showed that all eight mitogenomes comprised 12 protein-coding genes (PCGs) and two rRNAs; however, the mitogenomes differed in their genome sizes, GC content, tRNAs, non-coding regions and introns. Synteny analysis of the eight mitogenomes revealed a high degree of syntenic conservation in general, with some rearrangements and inversions. The average nucleotide identity (ANI) analysis of the eight mitogenomes indicated Oedogonium dentireticulatum showed high similarity with Oedogonium sp3 (ANI of 96.32%). Most of the PCGs of the eight mitogenomes presented the conventional start codon ATG and stop codon TAR (TAA/TAG/TGA), and the synonymous codon preferences were conserved. Phylogenetic results indicated that Oedogonium was polyphyletic, and species of Oedocladium clustered with Oedogonium, while the position of B. rectangularis var. hiloensis was uncertain for the incongruent phylogenetic results. Statistical analyses of substitution rates demonstrated no significant differences among the three genera, and the dN/dS ratios based on branch model showed that cob, cox1 and nad4 of Oedocladium prescottii and B. rectangularis var. hiloensis were putative fast-evolving genes. These findings suggested that the traditional taxonomy of Oedogoniales did not define natural groups, and that species of Oedocladium and Bulbochaete may have undergone rapid evolution.

Acknowledgements

This research was supported by the Wuhan Branch, Supercomputing Center, Chinese Academy of Sciences, China.

Disclosure statement

No potential conflict of interest was reported by the authors.

Supplementary material

The following supplementary material is accessible via the Supplementary Content tab on the article’s online page at https://doi.org/10.1080/09670262.2022.2035825.

Raw sequencing data of all species are available from the National Center for Biotechnology Information (NCBI) (https://www.ncbi.nlm.nih.gov/). Accession numbers of mitogenomes:

MW435175: https://www.ncbi.nlm.nih.gov/nuccore/MW435175

MW435176: https://www.ncbi.nlm.nih.gov/nuccore/MW435176

MW435177: https://www.ncbi.nlm.nih.gov/nuccore/MW435177

MW435178: https://www.ncbi.nlm.nih.gov/nuccore/MW435178

MW435179: https://www.ncbi.nlm.nih.gov/nuccore/MW435179

MW435180: https://www.ncbi.nlm.nih.gov/nuccore/MW435180

MW435181: https://www.ncbi.nlm.nih.gov/nuccore/MW435181

Supplementary table S1. Partition scheme of 12 concatenated mitogenome protein-coding genes used in this study.

Supplementary table S2. The start codon and stop codon of the 12 PCGs of the eight Oedogoniales species.

Supplementary table S3. The nonsynonymous (dN) and synonymous substitution (dS) rate of all the 12 PCGs of of the eight Oedogoniales species.

Supplementary table S4. The p values for pairwise comparation of the nonsynonymous (dN) and synonymous substitution (dS) rate among the three genera.

Supplementary figures S1–S7. Gene maps of the seven Oedogoniales mitochondrion genomes. Supplementary figure S1. Gene map of Oedogonium crispum mitochondrion genome. Supplementary figure S2. Gene map of Oedogonium sp. (FACHB-3317) mitochondrion genome. Supplementary figure S3. Gene map of Oedogonium dentireticulatum mitochondrion genome. Supplementary figure S4. Gene map of Oedogonium sp. (FACHB-3311) mitochondrion genome. Supplementary figure S5. Gene map of Oedogonium sp. (FACHB-3313) mitochondrion genome.

Supplementary figure S6. Gene map of Oedogonium capilliforme mitochondrion genome. Supplementary figure S7. Gene map of Oedocladium prescottii mitochondrion genome. Arrows show the direction of transcription. The same colour block shows the functional gene group (legend at bottom left). Transfer RNAs are represented by their one-letter amino acid code. The grey circle on the inside shows a graph of the GC content.

Supplementary figure S8. Heat map of ANI values of the eight Oedogoniales mitochondrion genomes.

Supplementary figure S9. Phylogenetic tree based on 18S rDNA sequences based on BI and ML method. Numbers on the left and right side at the branches represent ultrafast bootstrap inferred by Bayesian posterior probabilities (≥ 0.5) and IQTREE (≥ 50%), respectively. Branch lengths are proportional to the genetic distances, which are indicated by the scale bar.

Author contributions

Q. Xiong: original concept, culture experiments, data analysis, writing and editing manuscript; J. Wang: sample collecting; Y. Hu: editing manuscript; Q. Wang: editing manuscript; G. Liu: editing manuscript; Z. Hu: editing manuscript.

Additional information

Funding

This work was supported by Key Research Program of Frontier Sciences, CAS (Grant No. QYZDY-SSWSMC029-6) and the National Natural Science Foundation of China (grant no. 31750001).