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Nucleomorph Karyotype Diversity in the Freshwater

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Nucleomorph Karyotype Diversity in the Freshwater J. Phycol. 44, 11–14 (2008) Ó 2008 Phycological Society of America DOI: 10.1111/j.1529-8817.2007.00434.x NUCLEOMORPH KARYOTYPE DIVERSITY IN THE FRESHWATER CRYPTOPHYTE GENUS CRYPTOMONAS1 Kyle D. Phipps, Natalie A. Donaher, Christopher E. Lane, and John M. Archibald2 Canadian Institute for Advanced Research, Integrated Microbial Biodiversity Program, Department of Biochemistry and Molecular Biology, Dalhousie University, Sir Charles Tupper Medical Building, 5850 College Street, Halifax, Nova Scotia B3H 1X5, Canada Cryptophytes are unicellular, biflagellate algae et al. 2004). This primary endosymbiotic event pro- with plastids (chloroplasts) derived from the uptake duced the first primary plastid-containing algae, of a red algal endosymbiont. These organisms are which ultimately gave rise, through vertical evolu- unusual in that the nucleus of the engulfed red alga tion, to the red, green, and glaucophyte algae persists in a highly reduced form called a nucleo- (Archibald and Keeling 2002, 2005, Palmer 2003, morph. Nucleomorph genomes are remarkable in Keeling 2004). More recently, plastids have moved their small size (<1,000 kilobase pairs [kbp]) and horizontally across the eukaryotic tree by the pro- high degree of compaction ( 1 kbp per gene). cess of secondary endosymbiosis, in which a primary Here, we investigated the molecular and karyotypic plastid-containing eukaryote is taken up by a non- diversity of nucleomorph genomes in members of the photosynthetic eukaryotic host cell (Archibald and genus Cryptomonas. 18S rDNA genes were amplified, Keeling 2002, Palmer 2003, Keeling 2004). The sequenced, and analyzed from C. tetrapyrenoidosa exact number of secondary endosymbioses that have Skuja CCAP979 ⁄ 63, C. erosa Ehrenb. emmend. Hoef- occurred during eukaryotic evolution is contentious. Emden CCAP979 ⁄ 67, Cryptomonas sp. CCAP979 ⁄ 52, However, it is thought that secondary endosymbiosis C. lundii Hoef-Emden et Melkonian CCAP979 ⁄ 69, has occurred at least twice and involved the uptake and C. lucens Skuja CCAP979 ⁄ 35 in the context of a of both red and green algal endosymbionts large set of publicly available nucleomorph 18S rDNA (Archibald and Keeling 2002, Palmer 2003, Keeling sequences. Pulsed-field gel electrophoresis (PFGE) 2004, Bodyl 2005). was used to examine the nucleomorph genome karyo- The cryptophytes are an important lineage of type of each of these strains. Individual chromo- secondary plastid-containing algae whose plastid is somes ranged from 160 to 280 kbp in size, with derived from a captured red alga (McFadden total genome sizes estimated to be 600–655 kbp. 1993). Cryptophytes are unusual in that they still Unexpectedly, the nucleomorph karyotype of Crypto- possess the vestigial nucleus of their eukaryotic monas sp. CCAP979 ⁄ 52 is significantly different from endosymbiont, referred to as a nucleomorph that of C. tetrapyrenoidosa and C. lucens, despite the (McFadden 1993, Archibald 2007). Molecular and fact that their 18S rDNA genes are >99% identical to karyotypic analyses have revealed that the nucleo- one another. These results suggest that nucleomorph morphs of cryptophytes, as well as those of an karyotype similarity is not a reliable indicator of evo- unrelated group of algae called chlorarachnio- lutionary affinity and provides a starting point for fur- phytes, possess the smallest eukaryotic genomes ther investigation of the fine-scale dynamics of reported thus far, with those in cryptophytes rang- nucleomorph genome evolution within members of ing from 450 to 845 kbp in size (Eschbach et al. the genus Cryptomonas. 1991, Rensing et al. 1994, Lane et al. 2006). All known nucleomorph genomes comprise three Key index words: Cryptomonas; cryptophyte; gen- miniature chromosomes (Gilson and McFadden ome evolution; nucleomorph; secondary endo- 2002, Archibald 2007), which can be resolved symbiosis using PFGE (Eschbach et al. 1991, Rensing et al. Abbreviations: GTR, general time reversible; ML, 1994, Lane and Archibald 2006, Lane et al. 2006). maximum likelihood; PFGE, pulsed-field gel elec- The nucleomorph genome of the model crypto- trophoresis phyte Guillardia theta has been sequenced and is 551 kbp in size, with a gene density of 1 kbp per gene and 44 instances of overlapping genes Eukaryotic cells first acquired photosynthesis (Douglas et al. 2001). Each chromosome end is through the engulfment and retention of a cyano- capped with an atypical telomere and subtelomeric bacterial endosymbiont >1 billion years ago (Yoon rDNA operons. These unusual features make cryp- tophyte nucleomorphs an appealing subject for the study of eukaryotic genome evolution and, in 1 particular, the process of genome reduction and Received 12 September 2007. Accepted 28 September 2007. compaction. 2Author for correspondence: e-mail [email protected]. 11 12 KYLED.PHIPPSETAL. The genus Cryptomonas is unique among crypto- visible under ethidium bromide staining for most of phyte genera in that it includes exclusively fresh- the Cryptomonas strains examined here (data not water species, as well as the only species containing shown), likely due to the exceedingly small fraction a leucoplast (i.e., a nonphotosynthetic plastid). Cryp- of total cellular DNA that is of nucleomorph origin. tomonas paramecium has been shown to possess the However, Southern hybridization with an 18S rDNA smallest nucleomorph genome of known crypto- probe produced positive hybridization signals from phytes ( 450 kbp; Rensing et al. 1994) and resides the nucleomorph chromosomes, due to the fact that within a clade of species that appear to have ele- rDNA operons are a characteristic feature of nucleo- vated rates of nucleomorph sequence evolution (Hoef- morph chromosome ends (Fig. 2). Extensive cross- Emden et al. 2002, Hoef-Emden and Melkonian hybridization to the nuclear chromosomes of most 2003, Hoef-Emden 2005). These features make species was also apparent, as seen previously Cryptomonas an intriguing group for the comparative (Rensing et al. 1994, Lane et al. 2006). study of genome reduction and gene transfer from Considerable nucleomorph karyotype variation the nucleomorph to the host genome. Here, we pres- was observed among the five strains, with individual ent the first survey of nucleomorph karyotype diver- chromosomes ranging from 160 to 280 kbp (Fig. 2). sity within the genus Cryptomonas. Our results indicate Cryptomonas erosa, C. lucens, and C. tetrapyrenoidosa that nucleomorph genome size varies considerably were determined to possess similar karyotypes, with within this lineage, even among closely related three similarly sized chromosomes and total genome species. sizes ranging from 635 to 655 kbp (Fig. 2). Inter- Cryptophyte cultures were obtained from the estingly, Cryptomonassp. 979 ⁄ 52 and C. lundii possess Culture Collection of Algae and Protozoa (CCAP; highly distinct karyotypes, despite the fact that their Dunbeg, Argyll, UK). Nucleomorph-specific primers 18S rDNA genes share 99.5% sequence identity with were used to amplify, clone, and sequence 18S those of C. lucens and C. tetrapyrenoidosa. Cryptomonas rDNA genes from four cryptophyte species (as in sp. 979 ⁄ 52 contains three very dissimilarly sized Lane et al. 2006)—C. tetrapyrenoidosa CCAP979 ⁄ 63 chromosomes of 160, 200, and 280 kbp but (GenBank accession EU135976), Cryptomonas sp. maintains a total genome size of 640 kbp. The 18S 979 ⁄ 52 (EU135977), C. lundii CCAP979 ⁄ 69 rDNA and karyotype results for this species were (EU135975), and C. lucens CCAP979 ⁄ 35 confirmed using two independent cell cultures, rul- (EU135974)—whereas data from C. erosa ing out the possibility of DNA contamination. Sur- CCAP979 ⁄ 67 (AM396361) were already available. A prisingly, hybridization to C. lundii chromosomal maximum-likelihood (ML) phylogenetic tree was DNA produced a single, slightly diffuse hybridizing constructed using the general-time-reversible (GTR) band. This finding raises the following possibilities: model in PhyML (Guindon and Gascuel 2003) with (i) the C. lundii nucleomorph genome has fewer four rate categories and an additional invariable- than three chromosomes, (ii) the genome contains rates category. Parameters were estimated from the chromosomes that lack 18S rDNA genes (as has data, and 1,000 bootstrap replicates were performed been reported for members of the genus Hemiselmis to assess the reliability of the resulting topology. [Lane and Archibald 2006]), or (iii) C. lundii has Phylogenetic analysis of these sequences in the nucleomorph chromosomes of sufficiently similar context of a range of cryptophyte 18S rDNA size so as to be inseparable under the electropho- sequences obtained from GenBank revealed that retic conditions used in this study. Given that all C. tetrapyrenoidosa, Cryptomonas sp. 979 ⁄ 52, C. lundii, known cryptophyte (and chlorarachniophyte) nucle- and C. lucens group within a closely related clade, omorph genomes possess three chromosomes supported by a bootstrap value of 99% (Fig. 1) and (Archibald 2007), we favor the latter scenario and an average nucleomorph 18S rDNA sequence iden- tentatively assign a nucleomorph genome size of tity of 99.5%. Of all five strains examined here using 600 kbp to C. lundii (Fig. 2). PFGE, only C. erosa was resolved outside of the main The genus Cryptomonas is one of the least under- Cryptomonas clade, sharing 93% sequence identity stood groups of cryptophytes from the perspective with the other four strains. Collectively, all five of nucleomorph genome size diversity (Rensing sequences were distinct from the nonphotosynthetic
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