Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (Rhodophyta)
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RESEARCH ARTICLE
Open Access
Potential causes and consequences of rapid mitochondrial genome evolution in thermoacidophilic Galdieria (Rhodophyta) Chung Hyun Cho1†, Seung In Park1†, Claudia Ciniglia2, Eun Chan Yang3, Louis Graf1, Debashish Bhattacharya4 and Hwan Su Yoon1*
Abstract Background: The Cyanidiophyceae is an early-diverged red algal class that thrives in extreme conditions around acidic hot springs. Although this lineage has been highlighted as a model for understanding the biology of extremophilic eukaryotes, little is known about the molecular evolution of their mitochondrial genomes (mitogenomes). Results: To fill this knowledge gap, we sequenced five mitogenomes from representative clades of Cyanidiophyceae and identified two major groups, here referred to as Galdieria-type (G-type) and Cyanidium-type (C-type). G-type mitogenomes exhibit the following three features: (i) reduction in genome size and gene inventory, (ii) evolution of unique protein properties including charge, hydropathy, stability, amino acid composition, and protein size, and (iii) distinctive GC-content and skewness of nucleotides. Based on GC-skew-associated characteristics, we postulate that unidirectional DNA replication may have resulted in the rapid evolution of G-type mitogenomes. Conclusions: The high divergence of G-type mitogenomes was likely driven by natural selection in the multiple extreme environments that Galdieria species inhabit combined with their highly flexible heterotrophic metabolism. We speculate that the interplay between mitogenome divergence and adaptation may help explain the dominance of Galdieria species in diverse extreme habitats. Keywords: Cyanidiophyceae, Extremophile, Mitogenome evolution, Protein divergence, Mitochondrial DNA replication
Background Acidic hot springs environments can place severe stresses on unicellular organisms due to the high temperature, low pH, and elevated heavy-metal concentrations [1]. Most hot springs biodiversity is comprised of prokaryotes, with only a few eukaryotes able to compete successfully in these extreme habitats [2, 3]. The * Correspondence: [email protected] † Chung Hyun Cho and Seung In Park contributed equally to this work. 1 Department of Biological Sciences, Sungkyunkwan University, Suwon 16419, South Korea Full list of author information is available at the end of the article
unicellular red algal class, Cyanidiophyceae, is a wellknown group of extremophilic eukaryotes that thrives in acidic (pH 0.5–3.0) and high temperature (50–55 °C) habitats [4, 5]. Cyanidiophyceae have traditionally been reported from volcanic regions around the world [6–8], whereas some mesophilic species (e.g., Cyanidium chilense) are found in moderately acidic caves (pH 5–7) around volcanic regions in Chile, Italy, France, Israel, and Turkey [4, 9–12]. Cyanidiophyceae is the earliest diverging red algae lineage, having split from other Rhodophyta about 1.5 billion years ago [5, 13]. Due to
© The Author(s). 2020 Open Access This article is licensed under a Creative Commons At
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