The Ghost Plastid of Choreocolax Polysiphoniae
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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/272240511 The ghost plastid of Choreocolax polysiphoniae Article in Journal of Phycology · February 2015 DOI: 10.1111/jpy.12283 CITATIONS READS 29 287 3 authors: Eric Salomaki Katie Nickles Institute of Parasitology Biology Centre, ASCR University of Rhode Island 22 PUBLICATIONS 219 CITATIONS 4 PUBLICATIONS 32 CITATIONS SEE PROFILE SEE PROFILE Christopher E Lane University of Rhode Island 89 PUBLICATIONS 7,320 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Evolution of Parasitism in Red Algae View project Bermuda seaweed barcode project View project All content following this page was uploaded by Eric Salomaki on 24 July 2018. The user has requested enhancement of the downloaded file. J. Phycol. *, ***–*** (2015) © 2015 Phycological Society of America DOI: 10.1111/jpy.12283 L ETTER THE GHOST PLASTID OF CHOREOCOLAX POLYSIPHONIAE Eric D. Salomaki, Katie R. Nickles and Christopher E. Lane Parasitism has evolved innumerable times among eukaryotes. Red algal parasites alone have independently evolved over 100 times. The accepted evolutionary paradigm proposes that red algal parasites arise by first infecting a close relative and over time diversifying and infecting more distantly related species. This provides a natural evolutionary gradient of relationships between hosts and parasites that share a photosynthetic common ancestor. Upon infection, the parasite deposits its organelles into the host cell and takes over, spreading through cell-cell connections. Microscopy and molecular studies have demonstrated that the parasites do not maintain their own plastid, but rather abscond with a dedifferentiated host plastid as they pack up spores for dispersal. We sequenced a ~90 kb plastid genome from the parasite Choreocolax polysiphoniae, which has lost genes for light harvesting and photosynthesis. Furthermore, the presence of a native C. polysiphoniae plastid indicates that not all red algal parasites follow the same evolutionary pathway to parasitism. Along with the 167 kb plastid genome of its host, Vertebrata lanosa, these plastids are the first to be sequenced from the Ceramiales. RED ALGAL PARASITE EVOLUTION 1985, 1987, 1995, Goff and Zucca- non-photosynthetic plastid in rello 1994). The resulting hetero- C. polysiphoniae, indicates that mul- With over 100 extant species of karyotic host cell rapidly increases tiple evolutionary pathways to par- parasitic red algae (Blouin and carbohydrate production and asitism exist among red algae. Lane 2012, Salomaki and Lane starch formation, becoming 2014), most of which evolved enlarged (Goff and Coleman independently, red algae are a DESCRIPTIONS OF THE PLASTIDS 1987). The parasite eventually spectacular group to investigate directs the host to form spores, Vertebrata lanosa is a multicellu- the evolutionary mechanism by which will be released to start the lar polysiphonious red alga that which a species transitions from cycle again (Goff and Coleman belongs to the Rhodomelaceae free-living to parasitic. Shortly 1984b, Goff and Zuccarello 1994). (Fig. S1 in the Supporting Infor- after the discovery of red algal Interestingly, all red algal para- mation), and like other red algae parasites, phycologists postulated sites studied, including specimens with published plastid sequences, that parasites arise sympatrically from three different orders, have is a canonical photosynthetic red and infect the species with which lost their own plastid. Instead of alga. At 167 kilobases (kb) in they share their most recent com- maintaining their native plastid, length, the V. lanosa plastid gen- mon ancestry (Setchell 1918). they incorporate a dedifferentiat- ome (GenBank accession Subsequent molecular studies ed host plastid into their spores KP308097) is slightly smaller than have provided additional support (Goff and Coleman 1995). those previously sequenced from for this hypothesis (Goff and Until now, only the plastids of florideophytes, which range from Coleman 1987, Goff et al. 1996, red algal adelphoparasites (adel- 178 kb (Calliarthron tuberculosum) Zuccarello et al. 2004, Kurihara pho is Greek for “kin”) that share to 191 kb (Grateloupia taiwanensis; et al. 2010). These red algal para- a recent common ancestor with DePriest et al. 2013, Janouskovec sites take advantage of the close their host have been examined. et al. 2013). The V. lanosa plastid relationship with their host in Here, we describe the plastid of encodes 193 protein-coding their unique infection mecha- Choreocolax polysiphoniae Reinsch, a genes, the 16S, 23S, and 5S nism. parasite that is evolutionarily dis- rRNAs, 27 tRNAs (Fig. S1), and is Elegant studies by Goff and col- tant from its host (termed an allo- similar to other florideophyte leagues provided the fundamental parasite), and that of its host plastid genomes in gene content understanding of red algal para- Vertebrata lanosa (Linnaeus) T.A. and arrangement (Fig. S2 in the site biology and how they interact Christensen. These data reveal the Supporting Information). with their hosts. Upon infection, parasite-host plastid interactions Choreocolax polysiphoniae is also a red algal parasites fuse with a host may be quite different in allopara- member of the Rhodomelaceae; cell and deposit their cellular con- sites. The presence of a native however, it is an obligate parasite tents (Goff and Coleman 1984a, 1 2 of V. lanosa, which appears as a genes, 3 rRNAs, and 24 tRNAs. All photosynthesis, genes involved in multicellular unpigmented erum- 71 protein-coding genes are amino acid, fatty acid, isoprene, pent pustule growing from the shared with the V. lanosa plastid. and protein biosynthesis, tran- V. lanosa thallus (Fig. S1). In the However, petF is the only photo- scription and translation as well as course of gathering genome-scale synthesis-related protein encoded other cellular maintenance, are data from C. polysiphoniae, a 90 kb by the C. polysiphoniae plastid. In conserved. contig with high coverage (8159) C. polysiphoniae,asinChlamydo- The C. polysiphoniae ftsH gene, emerged from the data. Closer monas reinhardtii, it is likely to which is involved in photosystem examination revealed that the serve as an electron carrier in II repair, is missing the first ~150 contig represents a highly additional metabolic pathways residues, however, the conserva- reduced plastid genome sequence (Happe and Naber 1993, Jacobs tion of the remaining 452 amino (GenBank accession KP308096) in et al. 2009). Although the C. po- acid residues does not indicate C. polysiphoniae (Fig. 1). The plas- lysiphoniae plastid is no longer a loss of selection pressure on tid encodes 71 protein-coding capable of light harvesting and the gene. Conversely, only the ETTER L Prototheca clpP minD Vertebrata lanosa infA atpA atpF atpB atpH acsF gltB psaE psbX ycf4 atpE atpI apcA groEL psaF psbY ycf20 apcB infB pasI psbZ ycf21 apcD mat psaJ rbcL ycf22 accA rpl22 apcE moeB psaK rbcR ycf23 accB rpl27 apcF nblA psaL rbcS ycf33 acpP rpl29 rpl32 cysT argB ntcA psaM rpl9 ycf34 dnaB rpl31 rpl19 accD rps18 ycf1 atpD ompR psb28 rpl24 ycf35 dnaK rps6 rps9 ftsH atpG pbsA psb30 rpl28 ycf36 fabH rps10 rpl5 bas1 petA psbA rpl33 ycf39 hisS rps13 rpl12 rpl16 rps8 rpl14 rps19 Helicosporidium carA petB psbB rpl34 ycf45 ilvB secA rpl20 rpl2 rps12 rpoB ccs1 petD psbC rpl35 ycf46 ilvH secY rpoA rpl36 rps11 rpoC1 ccsA petG psbD rpoZ ycf52 infC sufC rps14 rps3 rrl rpoC2 cemA petJ psbE rps1 ycf53 odpA trpA tilS rps4 rrf tufA cfxQ petL psbF rps20 ycf54 odpB trpG rps7 rrs chlI petM psbH secG ycf55 petF tsf cpcA petN psbI syfB ycf56 rne ycf19 rpl23 cpcB pgmA psbJ tatC ycf63 rpl1 ycf29 rps2 cpcG preA psbK thiG ycf65 rpl3 ycf38 cpeA psaA psbL thiS rpl13 ycf60 clpC rps5 rpoD cpeB psaB psbN trxA rpl18 ycf80 rpl4 rps16 ycf24 dsbD psaC psbT upp rpl21 rpl6 sufB Apicoplast ftrB psaD psbV ycf3 Choreocolax polysiphoniae rpl11 rps17 Photosynthetic Processes Fatty Acid Biosynthesis Transport Conserved ORF of Unknown Function Iron-Sulfur Cluster Synthesis Amino Acid Biosynthesis Misc. Metabolic Function ATP synthase Carbohydrate Metabolism Housekeeping/Transcription/Translation FIG. 1. The plastid genome of the parasitic red alga, Choreocolax polysiphoniae is 90,243 basepairs and contains 71 coding genes (colored by protein function), the 5S, 16S, and 23S rRNAs (Red), and 24 tRNAs (Pink). All genes involved with photosynthetic functions, except petF, have been lost. The ftsH gene is truncated but may still be transcribed, however, gltB is a non-functional pseudogene (Yellow). The Venn diagram in the middle shows the plastid genome content of the free-living red alga, Vertebrata lanosa (red box), and its obligate para- site C. polysiphoniae (black box with gray shading). Additional boxes represent the green algal facultative parasite, Prototheca wickerhamii (dark green box), the green algal obligate parasite, Helicosporidium sp. (light green box), and a composite Apicoplast (blue box). Genes are color coded by protein function. 3 remnants of gltB are detectable Moore 2013), have been lost in due to the parasite relying on the using a Basic Local Alignment C. polysiphoniae. However, the uni- host for light harvesting and car- Search Tool (BLAST). Unlike the versal plastid amplicon (UPA) bohydrate production. conservation observed in ftsH, the marker provided meaningful com- Despite the annular representa- gltB region of the plastid genome parative data for phylogenetics tion of the C.