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Chloroplast Phylogenomic Analysis of Chlorophyte Green Revised MS (EVOB-D-15-00320R2) Click here to download Manuscript Revised_MS.docx Click here to view linked References 1 2 3 4 5 6 7 8 9 10 Chloroplast phylogenomic analysis of chlorophyte green algae 11 identifies a novel lineage sister to the Sphaeropleales 12 13 (Chlorophyceae) 14 15 16 17 18 Research Article 19 20 21 22 23 Claude Lemieux*, Antony T. Vincent, Aurélie Labarre, Christian Otis, and 24 Monique Turmel 25 26 27 28 Institut de Biologie Intégrative et des Systèmes, Département de biochimie, de 29 microbiologie et de bio-informatique, Université Laval, Québec (Québec) Canada 30 31 32 33 34 35 36 37 38 39 40 Authors’ email addresses: [email protected] 41 [email protected] 42 [email protected] 43 44 [email protected] 45 [email protected] 46 47 48 49 50 51 52 *Corresponding Author: Claude Lemieux 53 Institut de Biologie Intégrative et des Systèmes 54 55 1030 ave de la médecine, Pavillon Marchand 56 Université Laval, Québec (QC) Canada G1V 0A6; 57 phone: 418-656-2131 ext. 5171; Fax: 418-656-7176. 58 59 60 61 62 63 64 65 1 2 2 3 4 5 Abstract 6 7 Background: The class Chlorophyceae (Chlorophyta) includes morphologically and 8 9 10 ecologically diverse green algae. Most of the documented species belong to the clade formed by 11 12 the Chlamydomonadales (also called Volvocales) and Sphaeropleales. Although studies based on 13 14 the nuclear 18S rRNA gene or a few combined genes have shed light on the diversity and 15 16 17 phylogenetic structure of the Chlamydomonadales, the positions of many of the monophyletic 18 19 groups identified remain uncertain. Here, we used a chloroplast phylogenomic approach to 20 21 22 delineate the relationships among these lineages. 23 24 25 Results: To generate the analyzed amino acid and nucleotide data sets, we sequenced the 26 27 28 chloroplast DNAs (cpDNAs) of 24 chlorophycean taxa; these included representatives from 16 29 30 of the 21 primary clades previously recognized in the Chlamydomonadales, two taxa from a 31 32 33 coccoid lineage (Jenufa) that was suspected to be sister to the Golenkiniaceae, and two 34 35 sphaeroplealeans. Using Bayesian and/or maximum likelihood inference methods, we analyzed 36 37 an amino acid data set that was assembled from 69 cpDNA-encoded proteins of 73 core 38 39 40 chlorophyte (including 33 chlorophyceans), as well as two nucleotide data sets that were 41 42 generated from the 69 genes coding for these proteins and 29 RNA-coding genes. The protein 43 44 45 and gene phylogenies were congruent and robustly resolved the branching order of most of the 46 47 investigated lineages. Within the Chlamydomonadales, 22 taxa formed an assemblage of five 48 49 50 major clades/lineages. The earliest-diverging clade displayed Hafniomonas laevis and the 51 52 Crucicarteria, and was followed by the Radicarteria and then by the Chloromonadinia. The 53 54 latter lineage was sister to two superclades, one consisting of the Oogamochlamydinia and 55 56 57 Reinhardtinia and the other of the Caudivolvoxa and Xenovolvoxa. To our surprise, the Jenufa 58 59 species and the two spine-bearing green algae belonging to the Golenkinia and Treubaria genera 60 61 62 63 64 65 1 3 2 3 4 were recovered in a highly supported monophyletic group that also included three taxa 5 6 7 representing distinct families of the Sphaeropleales (Bracteacoccaceae, Mychonastaceae, and 8 9 Scenedesmaceae). 10 11 12 Conclusions: Our phylogenomic study advances our knowledge regarding the circumscription 13 14 and internal structure of the Chlamydomonadales, suggesting that a previously unrecognized 15 16 lineage is sister to the Sphaeropleales. In addition, it offers new insights into the flagellar 17 18 19 structures of the founding members of both the Chlamydomonadales and Sphaeropleales. 20 21 22 Key Words: Chlorophyceae, Chlamydomonadales, Golenkiniaceae, Treubarinia, Jenufa genus, 23 24 25 Plastid genome, Flagellar apparatus 26 27 28 29 30 Background 31 32 33 The Chlorophyceae occupies the crown of the Chlorophyta, one of the two divisions of the 34 35 36 Viridiplantae [1]. This monophyletic class of green algae comprises five orders or main clades 37 38 [2, 3] that form two major lineages [4, 5]: the Chlamydomonadales (or Volvocales) + 39 40 Sphaeropleales (CS clade) and the Oedogoniales + Chaetophorales + Chaetopeltidales (OCC 41 42 43 clade). Members of the Chlorophyceae are found in a wide range of habitats and display diverse 44 45 cell organizations (unicells, coccoids, colonies, simple flattened thalli, unbranched and branched 46 47 48 filaments) [1, 6]. Their motile cells also exhibit variability at the level of the flagellar apparatus. 49 50 The flagellar basal bodies of most chlorophycean green algae are displaced in a clockwise (CW, 51 52 53 1-7 o'clock) direction or are directly opposed (DO, 12-6 o'clock). In the Chlamydomonadales 54 55 (often designated as the CW clade), biflagellates display a CW orientation of basal bodies, 56 57 whereas quadriflagellates harbor distinct and more complex flagellar apparatus ultrastructures [7, 58 59 60 8]. The vegetatively nonmotile unicellular or colonial taxa found in the Sphaeropleales (DO 61 62 63 64 65 1 4 2 3 4 clade) produce zoospores with two flagella arranged in a DO configuration [9]. Quadriflagellates 5 6 7 with the perfect DO configuration of flagellar bodies characterize the Chaetopeltidales [10], 8 9 whereas quadriflagellates from the Chaetophorales display a polymorphic arrangement in which 10 11 12 one pair of basal bodies has the DO configuration and the other is slightly displaced in a 13 14 clockwise orientation [11, 12]. The members of the Oedogoniales have an unusual flagellar 15 16 apparatus that is characterized by a stephanokont arrangement of flagella [13]. 17 18 19 The Chlamydomonadales, the largest order of the Chlorophyceae, contains about half of 20 21 the 3,336 species currently described in this class [14]. Phylogenetic studies based on the nuclear 22 23 24 18S rRNA gene [7, 15-22] and/or a few chloroplast genes (e.g. atpB, psaB, rbcL) [23-25] as well 25 26 as combined 18S and 26S rDNAs [26] have highlighted numerous chlamydomonadalean 27 28 29 lineages. In an exhaustive phylogenetic analysis of the 449 chlamydomonadalean 18S rDNA 30 31 sequences available in GenBank at the time, Nakada et al. [16] uncovered 21 primary clades 32 33 34 following the rules of PhyloCode. The sequences of the spine-bearing Golenkinia species were 35 36 used to root the phylogeny because a sister relationship between the Golenkiniaceae and the 37 38 Chlamydomonadales had been reported earlier [27] and also because the motile cells of these 39 40 41 two groups have a CW basal body configuration [28]. Nakada et al. [16] identified a sister 42 43 relationship for the strongly supported Xenovolvoxa and Caudivolvoxa superclades, which are 44 45 46 composed of four and six primary clades, respectively. All remaining clades were found to be 47 48 basal relative to these superclades, with the four deepest-branching lineages displaying 49 50 51 quadriflagellates (Hafnionomas, Treubarinia, Radicarteria, and Crucicarteria clades) as 52 53 originally described by Nozaki et al. [24]. The interrelationships between most of the primary 54 55 clades, however, received low statistical support and were influenced by the method used for 56 57 58 phylogenetic inference. Phylogenetic studies based on a combination of two or three genes 59 60 61 62 63 64 65 1 5 2 3 4 (atpB, psaB, rbcL, 18S and 26S rDNAs) yielded trees with improved statistical support for some 5 6 7 of the clades, but their topologies were variable depending on the gene data sets employed and 8 9 were generally in conflict with 18S rDNA phylogenies. One study based on 18S and 26S rDNAs 10 11 12 even called into question the alliance of the deep-branching Treubarinia clade with the 13 14 Chlamydomonadales [2]. 15 16 In the present investigation, we used a chloroplast phylogenomic approach to resolve 17 18 19 problematic relationships among the major chlamydomonadalean clades proposed by Nakada et 20 21 al. [16]. Our taxon sampling included representatives from 16 of the 21 primary clades as well as 22 23 24 two taxa from a coccoid lineage (Jenufa) that was suspected to be sister to the Golenkiniaceae 25 26 [19]. We undertook the partial or complete sequencing of 24 chlorophycean chloroplast genomes 27 28 29 in order to generate the analyzed amino acid and nucleotide data sets. The results of our 30 31 phylogenomic analyses enabled us to resolve the branching order of most of the investigated 32 33 34 clades. Unexpectedly, the two Jenufa species and the representatives of the Golenkiniaceae and 35 36 Treubarinia were recovered in a highly supported monophyletic group that also included the taxa 37 38 belonging to the Sphaeropleales. 39 40 41 42 43 44 Results 45 46 47 The 24 chlorophycean taxa that were selected for chloroplast DNA (cpDNA) sequencing are 48 49 listed in Table 1. As mentioned earlier, they represent 16 of the 21 primary clades proposed by 50 51 52 Nakada et al. [16] and also include two bona fide sphaeroplealean taxa representing the 53 54 Bracteacoccaceae and Mychonastaceae. When we undertook our study, the partial or complete 55 56 cpDNA sequences of only five taxa from the CS clade were available: Chlamydomonas 57 58 59 reinhardtii [29], Volvox carteri f. nagariensis [30], Chlamydomonas moewusii [5], Dunaliella 60 61 62 63 64 65 1 6 2 3 4 salina [31] and Scenedesmus obliquus [32]. We used the Roche 454 or Illumina platform to 5 6 7 sequence the chloroplast genomes of the examined taxa and obtained complete genome 8 9 sequences for 13 taxa (Table 1).
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