Phylogeographic characteristics of hypervariable regions in the mitochondrial genome of a cosmopolitan, bloom‐forming raphidophyte, Heterosigma akashiwo

Abstract

The global distribution of phytoplankton is defined by many events, including long‐term evolutionary processes and shorter time span processes (e.g., global climate change). Furthermore, human‐assisted, unintentional dispersion, including the transport of live fish and spat for aquaculture, and transfer of aquatic microorganisms contained in ship ballast water, may aid the spread of phytoplankton. To understand the phylogeographic history of a species, the development of useful molecular markers is crucial. We previously reported a hypervariable mitochondrial gene in the cosmopolitan bloom‐forming alga, Heterosigma akashiwo. In this study, we identified two additional hypervariable segments in the H. akashiwo mitochondrial genome, one a protein coding sequence, and the other an intergenic region, by comparing the whole mitogenomes of strains obtained from various geographic origins. Interestingly, the newly identified hypervariable protein coding sequence was a paralogue of the previously identified gene, and both sequences showed tendencies to correlate with latitude of geographic origin. However, the hypervariable intergenic sequence did not show a clear correlation with origin. Our results demonstrated that the protein coding sequences may serve as useful tools for understanding the phylogeographic history of H. akashiwo, and they may crucially function in adaptation of the species to the environment.

Intraspecies variation of the mitochondrial genome: An evaluation for phylogenetic approaches based on the conventional choices of genes and segments on mitogenome

“…troglodytes (the second-highest correlation is shown in Fig 3 [ 28 , 29 ]), and H . akashiwo (expressed correlation at intermediate levels [ 31 – 33 ]), and compared the results with previously published observations. For the comparison, the partial mtDNA whose phylogeny exhibited the highest correlation with that of the entire mtDNA ( Fig 3 ) was chosen for each organism.…”

“…Previously, our group demonstrated that two particularly variable protein-coding regions of H . akashiwo showed a strong association with their geographic origins, while other parts of mtDNA did not [ 31 – 33 ]. This may demonstrate that, at least in certain species, analyses on different parts of the mtDNA sequences yield varied phylogenetic insights.…”

“…graminearum (fungal plant pathogen causing fusarium head blight on wheat, barley, and rice and ear rot on maize [ 41 ]), Gallus (domestic red junglefowl [ 42 ]), H . akashiwo (a protist, causative species of harmful algal bloom [ 31 – 33 ]), Pan troglodytes (chimpanzee [ 43 ]), and Ursus arctos (brown bear [ 28 , 29 ]). Such datasets were not available from the plant kingdom.…”

“…Previous studies revealed that two of the hypothetical proteins code for homologous proteins [ 31 – 33 ]. In this study, analysis of the newly sequenced mtDNA of 12 strains combined with the previously analyzed dataset further confirmed that these two protein-coding sequences, hypervariable open reading frames 1 and 2 ( MtORFvar1 and 2), expressed particularly high sequence heterogeneities ( Fig 2H [ 31 – 33 ]). An intergenic region between large ribosomal RNA and a hypothetical protein, termed the ‘intergenic variable region’ in previous studies [ 31 – 33 ], is also particularly highly variable ( Fig 2H ), while the sequences of the region did not express isolation-by-distance [ 31 – 33 ].…”

“…However, several studies have demonstrated that the phylogenetic inferences obtained from the entire mtDNA and the partial sequences, both D-loop and protein-coding sequences, may be discordant in some cases [ 28 – 30 ]. In addition, we identified two hypervariable genes on the mtDNA of a protist, Heterosigma akashiwo , that code for two hypothetical proteins that are homologous to each other [ 31 – 33 ]. Interestingly, their sequences show association with the geographic origins of the isolates, while the rest of mtDNA did not show clear isolation-by-distance, demonstrating that the phylogenetic studies based on different segments of H .…”