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Massive and Widespread Organelle Genomic Expansion in the Green Algal Genus Dunaliella

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Massive and Widespread Organelle Genomic Expansion in the Green Algal Genus Dunaliella GBE Massive and Widespread Organelle Genomic Expansion in the Green Algal Genus Dunaliella Michael Del Vasto1, Francisco Figueroa-Martinez2, Jonathan Featherston3,4, Mariela A. Gonza´lez5, Adrian Reyes-Prieto2, Pierre M. Durand3,6, and David Roy Smith1,* 1Department of Biology, University of Western Ontario, London, Ontario, Canada 2Department of Biology, Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, University of New Brunswick, Fredericton, New Brunswick, Canada Downloaded from https://academic.oup.com/gbe/article-abstract/7/3/656/602266 by guest on 03 May 2019 3Department of Molecular Medicine and Sydney Brenner Institute for Molecular Biosciences, University of the Witwatersrand, Johannesburg, South Africa 4Agricultural Research Council, Biotechnology Platform, Pretoria, South Africa 5Departamento de Bota´nica, Facultad de Ciencias Naturales y Oceano´ graficas. Universidad de Concepcio´ n, Casilla, Concepcio´ n, Chile 6Department of Biodiversity and Conservation Biology, Faculty of Natural Sciences, University of the Western Cape, Belville, Cape Town, South Africa *Corresponding author: E-mail: [email protected]. Data deposition: Sequence data from this article have been deposited at GenBank under accession numbers KP691601, KP691602, KP696388, and KP696389. Accepted: February 4, 2015 Abstract The mitochondrial genomes of chlamydomonadalean green algae are renowned for their highly reduced and conserved gene repertoires, which are almost fixed at 12 genes across the entire lineage. The sizes of these genomes, however, are much more variable, with some species having small, compact mitochondrial DNAs (mtDNAs) and others having expanded ones. Earlier work demonstrated that the halophilic genus Dunaliella contains extremely inflated organelle genomes, but to date the mtDNA of only one isolate has been explored. Here, by surveying mtDNA architecture across the Chlamydomonadales, we show that various Dunaliella species have undergone massive levels of mitochondrial genomic expansion, harboring the most inflated, intron-dense mtDNAs available from chlorophyte green algae. The same also appears to be true for their plastid genomes, which are potentially among the largest of all plastid-containing eukaryotes. Genetic divergence data are used to investigate the underlying causes of such extreme organelle genomic architectures, and ultimately reveal order-of-magnitude differences in mitochondrial versus plastid mutation rates within Dunaliella. Key words: Chlamydomonas, intron, mitochondrial DNA, plastid DNA, Polytoma. Introduction mitochondrial DNAs (mtDNAs) are distended with repeats The mitochondrial genomes of chlamydomonadalean green and introns, and composed almost entirely of noncoding nu- algae (Chlorophyta, Chlorophyceae) are somewhat of a con- cleotides (Smith and Lee 2010). tradiction (Leliaert et al. 2012). On the one hand, they have One species with a particularly bloated mitochondrial the smallest gene contents of any known organelle genomes genome is Dunaliella salina—a unicellular biflagellate, which from the Archaeplastida (Plantae sensu lato), encoding 7–8 lives in hypersaline environments, can accumulate large proteins, 2 rRNAs, and 1–3 tRNAs (Smith, Hamaji, et al. 2013; amounts of -carotene, and is a prime candidate for biofuel Smith, Hua, et al. 2013), and they can also be very small production (Oren 2005). Complete mtDNA sequencing of (<13.5 kb) and compact (>80% coding) (Smith, Hua, et al. D. salina CCAP 19/18, isolated from the Hutt Lagoon in 2010). On the other hand, certain chlamydomonadalean Western Australia, revealed an unprecedentedly high intron ß The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact [email protected] 656 Genome Biol. Evol. 7(3):656–663. doi:10.1093/gbe/evv027 Advance Access publication February 6, 2015 Organelle Genome Expansion GBE density for a green alga (~1.5 intron per gene) as well as vast, rRNAs), and contain sections of overlapping gene order repeat-rich intergenic regions (Smith, Lee, et al. 2010). An (fig. 1). Moreover, in each of the algae the mitochondrial equally expanded genome was also uncovered in the plastid, large and small subunit rRNA genes are fragmented and implying that similar forces are shaping both organelle DNAs scrambled into six and three coding modules, respectively (Smith, Lee, et al. 2010). (fig. 1), which is a common theme throughout the order, Various studies have used chlamydomonadalean algae, in- with species from the Reinhardtinia clade (Nakada et al. cluding the model organism Chlamydomonas reinhardtii and 2008) displaying even greater levels of rRNA gene fragmen- its close multicellular relative Volvox carteri, to explore the tation (Smith, Hamaji, et al. 2013). Three of the four genomes evolution of genome size (e.g., Smith and Lee 2010). These also have notably high guanine and cytosine (GC) contents: investigations suggest that mutation rate, DNA maintenance 39% (C. leiostraca), 46.7% (D. salina CONC-001), 47.1% (D. Downloaded from https://academic.oup.com/gbe/article-abstract/7/3/656/602266 by guest on 03 May 2019 machineries, and random genetic drift have a major role in viridis CONC-002), and 55% (P. uvella). These elevated GC fashioning organelle chromosomes (Smith and Lee 2010; Hua values are not entirely unexpected: The Chlamydomonadales et al. 2012; Smith, Hamaji, et al. 2013). Such studies, how- is known to harbor species with exceptionally high mtDNA GC ever, have yet to be applied to Dunaliella species, and it is still compositions, including the colorless alga Polytomella unknown if other members of the genus have inflated organ- capuana (57.2%) as well as some members of the elle genomes. Lobochlamys genus (~50–65%; Smith 2012). That said, Here, we survey mitochondrial genome size and content D. salina CCAP 19/18, unlike its Chilean counterparts, has a within and outside the Dunaliella lineage. We show that al- low mitochondrial GC content (34.4%), underscoring that though the mtDNA gene repertoire is nearly fixed across the organelle nucleotide content can differ drastically even Chlamydomonadales, there is an approximately 4-fold varia- among closely related species and strains. tion in genome size and an 18-fold variation in intron content, Further inspection revealed even more differences among with Dunaliella species having among the most expanded the mitochondrial genomes. The D. viridis CONC-002 and mtDNAs of all explored green algae. The same is likely true D. salina CONC-001 mtDNAs, with respective lengths of for their plastid genomes as well. The levels of organelle DNA approximately 46 and 50 kb, are around 3–4-times larger divergence between distinct D. salina strains are used to in- than those of C. leiostraca (14 kb) and P. uvella (17.4 kb), vestigate the potential forces underpinning such massive levels and on average greater than 2-times larger than other avail- of genomic expansion. able chlamydomonadalean mtDNAs, despite mitochondrial gene content being almost identical across the entire lineage. What’s more, the C. leiostraca and P. uvella mtDNAs con- Sequencing New Chlamydomonadalean Mitochondrial tain no introns, are densely packed (30% noncoding), and Genomes have matching gene orders, whereas D. viridis CONC-002 has As part of an ongoing, collaborative initiative, we 13 introns and D. salina CONC-001 has 17, and both species have been sequencing and characterizing organelle ge- are distended with noncoding mtDNA (>70%) and have nomes from diverse chlamydomonadalean species differing gene orders (fig. 1). In fact, the mtDNA of the (Hamaji et al. 2013; Smith, Hamaji, et al. 2013). Among Chilean D. salina described here is almost twice as large as these species are two distinct Dunaliella isolates, which the previously reported mtDNA of the Australian D. salina were collected from the La Rinconada hypersaline pond CCAP 19/18 (~50 kb vs. 28.3 kb), which, like the Chilean in the Atacama Desert in northern Chile: D. salina strain, also has an abundance of introns (18) (fig. 1; Smith, CONC-001 and Dunaliella viridis CONC-002 (Go´ mez- Lee, et al. 2010). Silva et al. 1990; Gonza´ lez et al. 1999; Go´ mez and In all, 48 putative introns are distributed among the three Gonza´ lez 2005). Closely related to Dunaliella are two sequenced Dunaliella mitochondrial genomes, representing other algae that we have also been investigating: the approximately 65% of all identified mitochondrial introns freshwater flagellate Chlamydomonas leiostraca SAG from the Chlamydomonadales. When looking at the location 11-49 and the free-living, nonphotosynthetic unicell of the Dunaliella introns, 28 have unique insertion sites (situ- Polytoma uvella UTEX 964, which are a model duo for ated within four different protein-coding genes and five dif- studying the loss of photosynthesis (Figueroa-Martinez ferent rRNA-coding modules), 17 are found in at least two of et al. 2015). the isolates, 11 are located in only a single isolate, and 8 Next-generation sequencing of total cellular DNA from contain an intronic open reading frame (ORF; fig. 1). All but these algae followed by mitochondrial genome assembly one
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