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Evolution of the Germline Actin Gene in Hypotrichous Ciliates: Multiple Nonscrambled Iess at Extremely Conserved Locations in Two Urostylids

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Evolution of the Germline Actin Gene in Hypotrichous Ciliates: Multiple Nonscrambled Iess at Extremely Conserved Locations in Two Urostylids The Journal of Published by the International Society of Eukaryotic Microbiology Protistologists Journal of Eukaryotic Microbiology ISSN 1066-5234 ORIGINAL ARTICLE Evolution of the Germline Actin Gene in Hypotrichous Ciliates: Multiple Nonscrambled IESs at Extremely Conserved Locations in Two Urostylids Tianbing Chena, Zhenzhen Yia, Jie Huangb & Xiaofeng Lina a Laboratory of Protozoology, School of Life Science, South China Normal University, Guangzhou 510631, China b Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China Keywords ABSTRACT Actin; ciliates; macronuclear; MDS; micronuclear. In hypotrichous ciliates, macronuclear chromosomes are gene-sized, and mi- cronuclear genes contain short, noncoding internal eliminated segments (IESs) Correspondence as well as macronuclear-destined segments (MDSs). In the present study, we Z. Yi and X. Lin, Key Laboratory of Ecology characterized the complete macronuclear gene and two to three types of mi- and Environmental Science in Guangdong cronuclear actin genes of two urostylid species, i.e. Pseudokeronopsis rubra Higher Education, South China Normal and Uroleptopsis citrina. Our results show that (1) the gain/loss of IES happens University, Guangzhou 510631, China frequently in the subclass Hypotrichia (formerly Stichotrichia), and high frag- Telephone/Fax number: +86 (0) 20-8521- mentation of germline genes does not imply for gene scrambling; and (2) the 0644; micronuclear actin gene is scrambled in the order Sporadotrichida but non- e-mail: [email protected]; [email protected] scrambled in the orders Urostylida and Stichotrichida, indicating the indepen- dent evolution of MIC-actin gene patterns in different orders of hypotrichs; (3) Macronuclear (/Micronuclear) actin is abbre- locations of MDS–IES junctions of micronuclear actin gene in coding regions viated as MAC(/MIC)-actin. IESn-n +1repre- are conserved among closely related species. sent the IES between MDSn and MDSn +1. Received: 7 November 2013; revised 16 June 2014; accepted July 8, 2014. doi:10.1111/jeu.12158 CILIATES are unicellular eukaryotes characterized by the and Klobutcher 2002; Prescott 1994). Assembly of these presence of cilia and nuclear dimorphism. Each cell con- MDSs generates a MAC with up to 20,000,000 amplified tains two types of nuclei: a diploid germline micronucleus gene-sized chromosomes in the class Spirotrichea (Baird (MIC) which is transcriptionally inactive except during sex- and Klobutcher 1991; Prescott 1994). ual conjugation, and a somatic macronucleus (MAC) which Macronuclear-destined segments within some micronu- is the primary source of gene transcripts (Prescott 1994). clear genes are scrambled in comparison to their linear The development of a new MAC from a MIC involves a arrangement in the macronucleus. It is estimated that series of chromosomal rearrangements, including DNA approximately one-third of the genes in Hypotrichia sensu elimination, fragmentation, and amplification (Jahn and Adl et al. (2012) (formerly Stichotrichia sensu Lynn 2008), Klobutcher 2002; Prescott 1994). These rearrangements a subclass of Spirotrichea, are scrambled (Cavalcanti et al. are extensive in three classes of ciliates: Armophorea, 2005). Among them, three genes have been extensively Phyllopharyngea, and Spirotrichea (the focus of this study). studied: actin I (Dalby and Prescott 2004; Greslin et al. Transposons and most intergenic spacer DNA, as well as 1989; Hogan et al. 2001; Mollenbeck€ et al. 2006), a-telo- intragenic spacer DNA, termed internal eliminated mere-binding protein (TEBP-a) (Mitcham et al. 1992; Pres- segments (IESs) are extensively eliminated from zygotic cott et al. 1998; Wong and Landweber 2006), and DNA chromosomes. In spirotrichous ciliates, the remaining polymerase a (DNA pol-a) (Chang et al. 2004, 2005; Hoff- DNA segments, called macronuclear-destined segments man and Prescott 1996, 1997; Landweber et al. 2000). (MDSs), occupy only 2–5% of the germline genome (Jahn However, conclusions about the evolution of these three © 2014 The Author(s) Journal of Eukaryotic Microbiology © 2014 International Society of Protistologists 188 Journal of Eukaryotic Microbiology 2015, 62, 188–195 Chen et al. Evolution of the Micronuclear Actin Gene genes vary. For example, it is reported that higher num- citrina, the micronuclear segments 33–35, 34–35 (Fig. 1) bers of MDSs are present in species with scrambled mi- were amplified using the SiteFinding-PCR products as cronuclear actin I (Hogan et al. 2001) and TEBP-a (Wong templates. After obtaining the IES sequence, MIC-specific and Landweber 2006) than in species with nonscrambled primers and MAC-based primers were used to recover the genes. By contrast, extensive fragmentation does not full length of these genes (Fig. 1). PCR products were imply for scrambling of the DNA poly-a gene (Chang et al. cloned into the pMDTM18-T vector (Takara Biotechnology, 2005). Dalian, China). M13F and M13R sequencing primers and To get a better understanding about the evolutionary species-specific internal primers were used for sequencing history of micronuclear genes within hypotrichous ciliates, in the Guangzhou branch of Beijing Genomics Institute we determined macronuclear and micronuclear structures (BGI, Beijing, China). of the actin gene from Pseudokeronopsis rubra and Urol- eptopsis citrina, which represent a divergent group from Phylogenetic analyses previously studied species (Hogan et al. 2001) as defined by SSU rDNA trees (Huang et al. 2014; Yi and Song Due to the high ambiguity of the noncoding sequence 2011). We compared our results with previous studies regions, only the coding sequences of the MAC-actin gene and discussed the evolution of micronuclear actin (MIC- (Table S1), of which the micronuclear versions are avail- actin) gene in hypotrichs. able, were used in the phylogenetic analysis. A SSU rDNA tree was also constructed using sequences from GenBank (Table S1). Maximum likelihood analyses, employing the MATERIALS AND METHODS GTR (General Time Reversible) substitution model and 1,000 bootstrap replicates, were conducted via CIPRES Cell culture and DNA extraction Science Gateway (http://www.phylo.org/sub_sections/ The cultures of P. rubra and U. citrina in this study were portal) using RaxML-HPC v7.2.5 (Stamatakis et al. 2008). isolated from marine habitats in China and have been kept in culture since several years ago (described in Huang RESULTS et al. 2010; Yi et al. 2008). Several cells were picked and cultures were established in autoclaved seawater with rice MAC-actin gene grains. Subsequently, cells were collected in a 1-liter bea- ker by filtering through a 20-lm filter to remove large par- Three and two overlapping PCR products of the MAC- ticulate debris. Once cells settled at the bottom of the actin gene were obtained from P. rubra and U. citrina, beaker, the supernatant was discarded and fresh auto- respectively (P-mac and U-mac, Fig. 1). One to five clones claved seawater was added. These steps were repeated from each segment were sequenced to obtain consensus several times to wash the cells and reduce the number of sequences. These have been submitted to GenBank under bacteria. After the final wash and removal of the superna- the accession numbers: KJ439789 (P. rubra), KJ439788 tant, the ciliates were starved overnight to digest remain- (U. citrina). ing bacteria within cells and then pelleted by Comparing sequences from different cloning products, centrifugation at 2655 g for 3 min before DNA extraction. 13 and 35 segregating sites are detected in the MAC-actin Total genomic DNA of the two species was extracted genes of P. rubra and U. citrina, respectively. For P. rubra, using the DNeasy Blood & Tissue Kit (Qiagen, cat. no. one occurs in the 50 leader region, three in the 30 trailer 69506, Hilden, Germany). Micronuclear DNA was isolated region, and nine in the CDS region. Of these polymor- from genomic DNA by gel electrophoresis following the phisms, three are nonsynonymous. In U. citrina, three method described in Katz et al. (2003), and purified using nucleotide polymorphisms occur in the 50 leader region, the QIAEX II Gel Extraction kit (Qiagen, cat. no. 20021). one in the 30 trailer region, and 31 fall into the CDS region, with seven being nonsynonymous. The complete MAC- actin chromosomes (excluding the telomere repeats) are PCR and cloning 1,429 and 1,415 bp in P. rubra and U. citrina, respectively. Complete macronuclear actin I (MAC-actin) gene They both encode a putative actin protein of 376 amino sequences of P. rubra and U. citrina were determined by acids. Similar to other hypotrichous species, the 50 leader telomere suppression PCR following procedures estab- and 30 trailer are AT-rich in both species. lished by Chang et al. (2004). Conventional PCR aiming to amplify the complete sequences of micronuclear genes MIC-actin gene failed with gel isolated MIC-DNA or BAL-31 Nuclease (New England Biolabs, cat. no. M0213, Hitchin, UK)-treated Three patterns (P-mic-a, P-mic-b, and P-mic-c) of the MIC- MIC-DNA templates, and only macronuclear segments actin gene were observed in P. rubra in the present study. were obtained. We performed walking PCR (SiteFinding- P-mic-a was sequenced in full length by primers 21 and PCR) to amplify the MIC-actin segment 13-SFP3 (Fig. 1) of 25, located on the ends of the gene, while the other two P. rubra (Tan et al. 2005). We also designed MIC-specific patterns were only partially sequenced, likely
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