in

The macronuclear genome of the Antarctic psychrophilic marine ciliate Euplotes focardii reveals new insights on molecular cold adaptation

  • 1.

    Pucciarelli, S. et al. Molecular cold-adaptation of protein function and gene regulation: the case for comparative genomic analyses in marine ciliated protozoa. Mar Genomics 2, 57–66. https://doi.org/10.1016/j.margen.2009.03.008 (2009).

    Article 
    PubMed 

    Google Scholar 

  • 2.

    Pucciarelli, S., Marziale, F., Di Giuseppe, G., Barchetta, S. & Miceli, C. Ribosomal cold-adaptation: characterization of the genes encoding the acidic ribosomal P0 and P2 proteins from the Antarctic ciliate Euplotes focardii. Gene 360, 103–110. https://doi.org/10.1016/j.gene.2005.06.007 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 3.

    Pucciarelli, S. & Miceli, C. Characterization of the cold-adapted alpha-tubulin from the psychrophilic ciliate Euplotes focardii. Extremophiles 6, 385–389. https://doi.org/10.1007/s00792-002-0268-5 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 4.

    Yang, G. et al. Characterization and comparative analysis of psychrophilic and mesophilic alpha-amylases from Euplotes species: a contribution to the understanding of enzyme thermal adaptation. Biochem Biophys Res Commun 438, 715–720. https://doi.org/10.1016/j.bbrc.2013.07.113 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 5.

    Prescott, D. M. The DNA of ciliated protozoa. Microbiol Rev 58, 233–267 (1994).

    CAS 
    Article 

    Google Scholar 

  • 6.

    Mollenbeck, M. & Klobutcher, L. A. De novo telomere addition to spacer sequences prior to their developmental degradation in Euplotes crassus. Nucleic Acids Res 30, 523–531 (2002).

    Article 

    Google Scholar 

  • 7.

    Swart, E. C. et al. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16,000 tiny chromosomes. PLoS Biol 11, e1001473. https://doi.org/10.1371/journal.pbio.1001473 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 8.

    Heyse, G., Jonsson, F., Chang, W. J. & Lipps, H. J. RNA-dependent control of gene amplification. Proc Natl Acad Sci U S A 107, 22134–22139. https://doi.org/10.1073/pnas.1009284107 (2010).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 9.

    Nowacki, M., Haye, J. E., Fang, W., Vijayan, V. & Landweber, L. F. RNA-mediated epigenetic regulation of DNA copy number. Proc Natl Acad Sci U S A 107, 22140–22144. https://doi.org/10.1073/pnas.1012236107 (2010).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Dayeh, V. R. et al. Comparing a ciliate and a fish cell line for their sensitivity to several classes of toxicants by the novel application of multiwell filter plates to Tetrahymena. Res Microbiol 156, 93–103. https://doi.org/10.1016/j.resmic.2004.08.005 (2005).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 11.

    Detrich, H. W., 3rd, Parker, S. K., Williams, R. C., Jr., Nogales, E. & Downing, K. H. Cold adaptation of microtubule assembly and dynamics. Structural interpretation of primary sequence changes present in the alpha- and beta-tubulins of Antarctic fishes. J Biol Chem 275, 37038–37047. https://doi.org/10.1074/jbc.M005699200 (2000).

  • 12.

    Manka, S. W. & Moores, C. A. Microtubule structure by cryo-EM: snapshots of dynamic instability. Essays Biochem 62, 737–751. https://doi.org/10.1042/EBC20180031 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 13.

    Inclan, Y. F. & Nogales, E. Structural models for the self-assembly and microtubule interactions of gamma-, delta- and epsilon-tubulin. J Cell Sci 114, 413–422 (2001).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Chiappori, F. et al. Structural thermal adaptation of beta-tubulins from the Antarctic psychrophilic protozoan Euplotes focardii. Proteins 80, 1154–1166. https://doi.org/10.1002/prot.24016 (2012).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 15.

    Marziale, F. et al. Different roles of two gamma-tubulin isotypes in the cytoskeleton of the Antarctic ciliate Euplotes focardii: remodelling of interaction surfaces may enhance microtubule nucleation at low temperature. FEBS J 275, 5367–5382. https://doi.org/10.1111/j.1742-4658.2008.06666.x (2008).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 16.

    Pucciarelli, S., Miceli, C. & Melki, R. Heterologous expression and folding analysis of a beta-tubulin isotype from the Antarctic ciliate Euplotes focardii. Eur J Biochem 269, 6271–6277 (2002).

    CAS 
    Article 

    Google Scholar 

  • 17.

    Gromer, S., Urig, S. & Becker, K. The thioredoxin system–from science to clinic. Med Res Rev 24, 40–89. https://doi.org/10.1002/med.10051 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 18.

    Birben, E., Sahiner, U. M., Sackesen, C., Erzurum, S. & Kalayci, O. Oxidative stress and antioxidant defense. World Allergy Organ J 5, 9–19. https://doi.org/10.1097/WOX.0b013e3182439613 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 19.

    Alin, P., Danielson, U. H. & Mannervik, B. 4-Hydroxyalk-2-enals are substrates for glutathione transferase. FEBS Lett 179, 267–270 (1985).

    CAS 
    Article 

    Google Scholar 

  • 20.

    Juganson, K. et al. Mechanisms of toxic action of silver nanoparticles in the protozoan Tetrahymena thermophila: From gene expression to phenotypic events. Environ Pollut 225, 481–489. https://doi.org/10.1016/j.envpol.2017.03.013 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 21.

    Clark, M. S., Fraser, K. P. & Peck, L. S. Antarctic marine molluscs do have an HSP70 heat shock response. Cell Stress Chaperones 13, 39–49. https://doi.org/10.1007/s12192-008-0014-8 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 22.

    Tomanek, L. The heat-shock response: its variation, regulation and ecological importance in intertidal gastropods (genus Tegula). Integr Comp Biol 42, 797–807. https://doi.org/10.1093/icb/42.4.797 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 23.

    Morimoto, R. I., Kline, M. P., Bimston, D. N. & Cotto, J. J. The heat-shock response: regulation and function of heat-shock proteins and molecular chaperones. Essays Biochem 32, 17–29 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • 24.

    Gonzalez-Aravena, M. et al. HSP70 from the Antarctic sea urchin Sterechinus neumayeri: molecular characterization and expression in response to heat stress. Biol Res 51, 8. https://doi.org/10.1186/s40659-018-0156-9 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 25.

    Hofmann, G. E., Buckley, B. A., Airaksinen, S., Keen, J. E. & Somero, G. N. Heat-shock protein expression is absent in the antarctic fish Trematomus bernacchii (family Nototheniidae). J Exp Biol 203, 2331–2339 (2000).

    CAS 
    Article 

    Google Scholar 

  • 26.

    La Terza, A., Papa, G., Miceli, C. & Luporini, P. Divergence between two Antarctic species of the ciliate Euplotes, E. focardii and E. nobilii, in the expression of heat-shock protein 70 genes. Mol Ecol 10, 1061–1067. https://doi.org/10.1046/j.1365-294x.2001.01242.x (2001).

  • 27.

    Klobutcher, L. A. & Farabaugh, P. J. Shifty ciliates: frequent programmed translational frameshifting in euplotids. Cell 111, 763–766 (2002).

    CAS 
    Article 

    Google Scholar 

  • 28.

    Lobanov, A. V. et al. Position-dependent termination and widespread obligatory frameshifting in Euplotes translation. Nat Struct Mol Biol 24, 61–68. https://doi.org/10.1038/nsmb.3330 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 29.

    Coordinators, N. R. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 45, D12–D17. https://doi.org/10.1093/nar/gkw1071 (2017).

    CAS 
    Article 

    Google Scholar 

  • 30.

    Pucciarelli, S. et al. Microbial consortium associated with the antarctic marine ciliate Euplotes focardii: an investigation from genomic sequences. Microb Ecol 70, 484–497. https://doi.org/10.1007/s00248-015-0568-9 (2015).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 31.

    Klobutcher, L. A. et al. Conserved DNA sequences adjacent to chromosome fragmentation and telomere addition sites in Euplotes crassus. Nucleic Acids Res 26, 4230–4240. https://doi.org/10.1093/nar/26.18.4230 (1998).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 32.

    Aeschlimann, S. H. et al. The draft assembly of the radically organized Stylonychia lemnae macronuclear genome. Genome Biol Evol 6, 1707–1723. https://doi.org/10.1093/gbe/evu139 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 33.

    Swart, E. C. (personal communication).

  • 34.

    Cavalcanti, A. R., Stover, N. A., Orecchia, L., Doak, T. G. & Landweber, L. F. Coding properties of Oxytricha trifallax (Sterkiella histriomuscorum) macronuclear chromosomes: analysis of a pilot genome project. Chromosoma 113, 69–76. https://doi.org/10.1007/s00412-004-0295-3 (2004).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 35.

    Lozupone, C. A., Knight, R. D. & Landweber, L. F. The molecular basis of nuclear genetic code change in ciliates. Curr Biol 11, 65–74. https://doi.org/10.1016/s0960-9822(01)00028-8 (2001).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 36.

    Salas-Marco, J. et al. Distinct paths to stop codon reassignment by the variant-code organisms Tetrahymena and Euplotes. Mol Cell Biol 26, 438–447. https://doi.org/10.1128/MCB.26.2.438-447.2006 (2006).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 37.

    Klobutcher, L. A. Sequencing of random Euplotes crassus macronuclear genes supports a high frequency of +1 translational frameshifting. Eukaryot Cell 4, 2098–2105. https://doi.org/10.1128/EC.4.12.2098-2105.2005 (2005).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 38.

    Wang, R., Xiong, J., Wang, W., Miao, W. & Liang, A. High frequency of +1 programmed ribosomal frameshifting in Euplotes octocarinatus. Sci Rep 6, 21139. https://doi.org/10.1038/srep21139 (2016).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 39.

    Turanov, A. A. et al. Genetic code supports targeted insertion of two amino acids by one codon. Science 323, 259–261. https://doi.org/10.1126/science.1164748 (2009).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 40.

    Maehigashi, T., Dunkle, J. A., Miles, S. J. & Dunham, C. M. Structural insights into +1 frameshifting promoted by expanded or modification-deficient anticodon stem loops. Proc Natl Acad Sci U S A 111, 12740–12745. https://doi.org/10.1073/pnas.1409436111 (2014).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 41.

    Miceli, C., Ballarini, P., Di Giuseppe, G., Valbonesi, A. & Luporini, P. Identification of the tubulin gene family and sequence determination of one beta-tubulin gene in a cold-poikilotherm protozoan, the antarctic ciliate Euplotes focardii. J Eukaryot Microbiol 41, 420–427. https://doi.org/10.1111/j.1550-7408.1994.tb06100.x (1994).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 42.

    Ricci, F. et al. The sub-chromosomic macronuclear pheromone genes of the ciliate Euplotes raikovi: comparative structural analysis and insights into the mechanism of expression. J Eukaryot Microbiol 66, 376–384. https://doi.org/10.1111/jeu.12677 (2019).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 43.

    Wang, R., Liu, J., Di Giuseppe, G. & Liang, A. UAA and UAG may Encode Amino Acid in Cathepsin B Gene of Euplotes octocarinatus. J Eukaryot Microbiol 67, 144–149. https://doi.org/10.1111/jeu.12755 (2020).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 44.

    Heaphy, S. M., Mariotti, M., Gladyshev, V. N., Atkins, J. F. & Baranov, P. V. Novel ciliate genetic code variants including the reassignment of all three stop codons to sense codons in condylostoma magnum. Mol Biol Evol 33, 2885–2889. https://doi.org/10.1093/molbev/msw166 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 45.

    Swart, E. C., Serra, V., Petroni, G. & Nowacki, M. Genetic codes with no dedicated stop codon: context-dependent translation termination. Cell 166, 691–702. https://doi.org/10.1016/j.cell.2016.06.020 (2016).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 46.

    Roy, B., Leszyk, J. D., Mangus, D. A. & Jacobson, A. Nonsense suppression by near-cognate tRNAs employs alternative base pairing at codon positions 1 and 3. Proc Natl Acad Sci U S A 112, 3038–3043. https://doi.org/10.1073/pnas.1424127112 (2015).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 47.

    Dunn, J. G., Foo, C. K., Belletier, N. G., Gavis, E. R. & Weissman, J. S. Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. Elife 2, e01179. https://doi.org/10.7554/eLife.01179 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 48.

    Frechin, M., Duchene, A. M. & Becker, H. D. Translating organellar glutamine codons: a case by case scenario?. RNA Biol 6, 31–34. https://doi.org/10.4161/rna.6.1.7564 (2009).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 49.

    Wilcox, M. & Nirenberg, M. Transfer RNA as a cofactor coupling amino acid synthesis with that of protein. Proc Natl Acad Sci U S A 61, 229–236. https://doi.org/10.1073/pnas.61.1.229 (1968).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Detrich, H. W. 3rd., Fitzgerald, T. J., Dinsmore, J. H. & Marchese-Ragona, S. P. Brain and egg tubulins from antarctic fishes are functionally and structurally distinct. J Biol Chem 267, 18766–18775 (1992).

    CAS 
    Article 

    Google Scholar 

  • 51.

    Detrich, H. W. 3rd., Johnson, K. A. & Marchese-Ragona, S. P. Polymerization of Antarctic fish tubulins at low temperatures: energetic aspects. Biochemistry 28, 10085–10093 (1989).

    CAS 
    Article 

    Google Scholar 

  • 52.

    Wloga, D. et al. Glutamylation on alpha-tubulin is not essential but affects the assembly and functions of a subset of microtubules in Tetrahymena thermophila. Eukaryot Cell 7, 1362–1372. https://doi.org/10.1128/EC.00084-08 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Eisen, J. A. et al. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4, e286. https://doi.org/10.1371/journal.pbio.0040286 (2006).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 54.

    Aury, J. M. et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature 444, 171–178. https://doi.org/10.1038/nature05230 (2006).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 55.

    Pucciarelli, S. et al. Distinct functional roles of beta-tubulin isotypes in microtubule arrays of Tetrahymena thermophila, a model single-celled organism. PLoS ONE 7, e39694. https://doi.org/10.1371/journal.pone.0039694 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 56.

    Pucciarelli, S. et al. Tubulin folding: the special case of a beta-tubulin isotype from the Antarctic psychrophilic ciliate Euplotes focardii. Polar Biol 36, 1833–1838. https://doi.org/10.1007/s00300-013-1390-9 (2013).

    Article 

    Google Scholar 

  • 57.

    Pucci, F. & Rooman, M. Physical and molecular bases of protein thermal stability and cold adaptation. Curr Opin Struct Biol 42, 117–128. https://doi.org/10.1016/j.sbi.2016.12.007 (2017).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 58.

    Aqvist, J., Isaksen, G. V. & Brandsdal, B. O. Computation of enzyme cold adaptation. Nat Rev Chem 1, 0051. https://doi.org/10.1038/s41570-017-0051 (2017).

    CAS 
    Article 

    Google Scholar 

  • 59.

    Lesser, M. P. Oxidative stress in marine environments: biochemistry and physiological ecology. Annu Rev Physiol 68, 253–278. https://doi.org/10.1146/annurev.physiol.68.040104.110001 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 60.

    McCord, J. M. & Fridovich, I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 244, 6049–6055 (1969).

  • 61.

    McCord, J. M. & Fridovich, I. Superoxide dismutase: the first twenty years (1968–1988). Free Radic Biol Med 5, 363–369 (1988).

    CAS 
    Article 

    Google Scholar 

  • 62.

    Miller, A. F. Superoxide dismutases: ancient enzymes and new insights. FEBS Lett 586, 585–595. https://doi.org/10.1016/j.febslet.2011.10.048 (2012).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 63.

    Benov, L. T. & Fridovich, I. Escherichia coli expresses a copper- and zinc-containing superoxide dismutase. J Biol Chem 269, 25310–25314 (1994).

    CAS 
    Article 

    Google Scholar 

  • 64.

    Steinman, H. M. & Ely, B. Copper-zinc superoxide dismutase of Caulobacter crescentus: cloning, sequencing, and mapping of the gene and periplasmic location of the enzyme. J Bacteriol 172, 2901–2910. https://doi.org/10.1128/jb.172.6.2901-2910.1990 (1990).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 65.

    Antonyuk, S. V., Strange, R. W., Marklund, S. L. & Hasnain, S. S. The structure of human extracellular copper-zinc superoxide dismutase at 1.7 A resolution: insights into heparin and collagen binding. J Mol Biol 388, 310–326. https://doi.org/10.1016/j.jmb.2009.03.026 (2009).

  • 66.

    Marklund, S. L. Extracellular superoxide dismutase and other superoxide dismutase isoenzymes in tissues from nine mammalian species. Biochem J 222, 649–655. https://doi.org/10.1042/bj2220649 (1984).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 67.

    Bannister, J. V., Bannister, W. H. & Rotilio, G. Aspects of the structure, function, and applications of superoxide dismutase. CRC Crit Rev Biochem 22, 111–180 (1987).

    CAS 
    Article 

    Google Scholar 

  • 68.

    James, E. R. Superoxide dismutase. Parasitol Today 10, 481–484. https://doi.org/10.1016/0169-4758(94)90161-9 (1994).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 69.

    Ferro, D. et al. Cu, Zn superoxide dismutases from Tetrahymena thermophila: molecular evolution and gene expression of the first line of antioxidant defenses. Protist 166, 131–145. https://doi.org/10.1016/j.protis.2014.12.003 (2015).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 70.

    Arnaiz, O. & Sperling, L. ParameciumDB in 2011: new tools and new data for functional and comparative genomics of the model ciliate Paramecium tetraurelia. Nucleic Acids Res 39, D632-636. https://doi.org/10.1093/nar/gkq918 (2011).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 71.

    Fink, R. C. & Scandalios, J. G. Molecular evolution and structure–function relationships of the superoxide dismutase gene families in angiosperms and their relationship to other eukaryotic and prokaryotic superoxide dismutases. Arch Biochem Biophys 399, 19–36. https://doi.org/10.1006/abbi.2001.2739 (2002).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 72.

    Lee, Y. M., Friedman, D. J. & Ayala, F. J. Superoxide dismutase: an evolutionary puzzle. Proc Natl Acad Sci U S A 82, 824–828. https://doi.org/10.1073/pnas.82.3.824 (1985).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 73.

    Pischedda, A. et al. Antarctic marine ciliates under stress: superoxide dismutases from the psychrophilic Euplotes focardii are cold-active yet heat tolerant enzymes. Sci Rep 8, 14721. https://doi.org/10.1038/s41598-018-33127-1 (2018).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 74.

    Yang, G. et al. Characterization of the first eukaryotic cold-adapted patatin-like phospholipase from the psychrophilic Euplotes focardii: Identification of putative determinants of thermal-adaptation by comparison with the homologous protein from the mesophilic Euplotes crassus. Biochimie 95, 1795–1806. https://doi.org/10.1016/j.biochi.2013.06.008 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 75.

    Li, J., Zhou, L., Lin, X., Yi, Z. & Al-Rasheid, K. A. Characterizing dose-responses of catalase to nitrofurazone exposure in model ciliated protozoan Euplotes vannus for ecotoxicity assessment: enzyme activity and mRNA expression. Ecotoxicol Environ Saf 100, 294–302. https://doi.org/10.1016/j.ecoenv.2013.08.021 (2014).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 76.

    Prast-Nielsen, S., Huang, H. H. & Williams, D. L. Thioredoxin glutathione reductase: its role in redox biology and potential as a target for drugs against neglected diseases. Biochim Biophys Acta 1262–1271, 2011. https://doi.org/10.1016/j.bbagen.2011.06.024 (1810).

    CAS 
    Article 

    Google Scholar 

  • 77.

    Kabani, M. & Martineau, C. N. Multiple hsp70 isoforms in the eukaryotic cytosol: mere redundancy or functional specificity?. Curr Genomics 9, 338–248. https://doi.org/10.2174/138920208785133280 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 78.

    La Terza, A., Miceli, C. & Luporini, P. The gene for the heat-shock protein 70 of Euplotes focardii, an Antarctic psychrophilic ciliate. Antarct. Sci. 16, 23–28. https://doi.org/10.1017/S0954102004001774 (2004).

    ADS 
    Article 

    Google Scholar 

  • 79.

    Chen, X. et al. Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors. Mol Ecol Resour 19, 1292–1308. https://doi.org/10.1111/1755-0998.13023 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 80.

    Chen, Z. et al. Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proc Natl Acad Sci U S A 105, 12944–12949. https://doi.org/10.1073/pnas.0802432105 (2008).

    ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 81.

    Li, Y. et al. Comparative transcriptomic analysis reveals gene expression associated with cold adaptation in the tea plant Camellia sinensis. BMC Genomics 20, 624. https://doi.org/10.1186/s12864-019-5988-3 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 82.

    Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. https://doi.org/10.1093/bioinformatics/btu170 (2014).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 83.

    Andrews, S. (2010).

  • 84.

    Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19, 455–477. https://doi.org/10.1089/cmb.2012.0021 (2012).

    MathSciNet 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 85.

    Nikolenko, S. I., Korobeynikov, A. I. & Alekseyev, M. A. BayesHammer: Bayesian clustering for error correction in single-cell sequencing. BMC Genomics 14 Suppl 1, S7. https://doi.org/10.1186/1471-2164-14-S1-S7 (2013).

  • 86.

    Gurevich, A., Saveliev, V., Vyahhi, N. & Tesler, G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 29, 1072–1075. https://doi.org/10.1093/bioinformatics/btt086 (2013).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 87.

    Boscaro, V., Husnik, F., Vannini, C. & Keeling, P. J. Symbionts of the ciliate Euplotes: diversity, patterns and potential as models for bacteria-eukaryote endosymbioses. Proc Biol Sci 286, 20190693. https://doi.org/10.1098/rspb.2019.0693 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 88.

    Serra, V. et al. Morphology, ultrastructure, genomics, and phylogeny of Euplotes vanleeuwenhoeki sp. nov. and its ultra-reduced endosymbiont “Candidatus Pinguicoccus supinus” sp. nov. Sci Rep 10, 20311. https://doi.org/10.1038/s41598-020-76348-z (2020).

  • 89.

    Stanke, M. et al. AUGUSTUS: ab initio prediction of alternative transcripts. Nucleic Acids Res 34, W435-439. https://doi.org/10.1093/nar/gkl200 (2006).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 90.

    Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323. https://doi.org/10.1186/1471-2105-12-323 (2011).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 91.

    Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676. https://doi.org/10.1093/bioinformatics/bti610 (2005).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 92.

    Gotz, S. et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 36, 3420–3435. https://doi.org/10.1093/nar/gkn176 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 93.

    Parra, G., Bradnam, K. & Korf, I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23, 1061–1067. https://doi.org/10.1093/bioinformatics/btm071 (2007).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 94.

    Laslett, D. & Canback, B. ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences. Nucleic Acids Res 32, 11–16. https://doi.org/10.1093/nar/gkh152 (2004).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 95.

    Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R. & Hofacker, I. L. The Vienna RNA websuite. Nucleic Acids Res 36, W70-74. https://doi.org/10.1093/nar/gkn188 (2008).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 96.

    Popenda, M. et al. Automated 3D structure composition for large RNAs. Nucleic Acids Res 40, e112. https://doi.org/10.1093/nar/gks339 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 97.

    Fu, L., Niu, B., Zhu, Z., Wu, S. & Li, W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152. https://doi.org/10.1093/bioinformatics/bts565 (2012).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 98.

    Li, W. & Godzik, A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659. https://doi.org/10.1093/bioinformatics/btl158 (2006).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 99.

    Shigematsu, M. et al. YAMAT-seq: an efficient method for high-throughput sequencing of mature transfer RNAs. Nucleic Acids Res 45, e70. https://doi.org/10.1093/nar/gkx005 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 100.

    Bushnell, B., Rood, J. & Singer, E. BBMerge: accurate paired shotgun read merging via overlap. PLoS ONE 12, e0185056. https://doi.org/10.1371/journal.pone.0185056 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 101.

    Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. 2011 17, 3. https://doi.org/10.14806/ej.17.1.200 (2011).

  • 102.

    Holmes, A. D., Howard, J. M., Chan, P. P. & Lowe, T. M. tRNA Analysis of eXpression (tRAX): A tool for integrating analysis of tRNAs, tRNA-derived small RNAs, and tRNA modifications. (Submitted) (2020).

  • 103.

    Sievers, F. & Higgins, D. G. Clustal omega. Curr Protoc Bioinformatics 48, 3 13 11–16. https://doi.org/10.1002/0471250953.bi0313s48 (2014).

  • 104.

    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547–1549. https://doi.org/10.1093/molbev/msy096 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 105.

    Webb, B. & Sali, A. Comparative protein structure modeling using MODELLER. Curr Protoc Bioinform. 54, 5 6 1–5 6 37. https://doi.org/10.1002/cpbi.3 (2016).

  • 106.

    Waterhouse, A. et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 46, W296–W303. https://doi.org/10.1093/nar/gky427 (2018).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 107.

    Ichikawa, M. et al. Tubulin lattice in cilia is in a stressed form regulated by microtubule inner proteins. Proc Natl Acad Sci U S A 116, 19930–19938. https://doi.org/10.1073/pnas.1911119116 (2019).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 108.

    Chaaban, S. et al. The Structure and Dynamics of C. elegans Tubulin Reveals the Mechanistic Basis of Microtubule Growth. Dev Cell 47, 191–204 e198. https://doi.org/10.1016/j.devcel.2018.08.023 (2018).

  • 109.

    Kikkawa, M. et al. Switch-based mechanism of kinesin motors. Nature 411, 439–445. https://doi.org/10.1038/35078000 (2001).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • 110.

    Howes, S. C. et al. Structural differences between yeast and mammalian microtubules revealed by cryo-EM. J Cell Biol 216, 2669–2677. https://doi.org/10.1083/jcb.201612195 (2017).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 111.

    Ma, M. et al. Structure of the Decorated Ciliary Doublet Microtubule. Cell 179, 909–922 e912. https://doi.org/10.1016/j.cell.2019.09.030 (2019).

  • 112.

    Abraham, M. J. et al. GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001 (2015).

    ADS 
    Article 

    Google Scholar 

  • 113.

    Morrison, T. B., Weis, J. J. & Wittwer, C. T. Quantification of low-copy transcripts by continuous SYBR Green I monitoring during amplification. Biotechniques 24, 954–958, 960, 962 (1998).

  • 114.

    Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45. https://doi.org/10.1093/nar/29.9.e45 (2001).

    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 115.

    Pfaffl, M. W., Horgan, G. W. & Dempfle, L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30, e36. https://doi.org/10.1093/nar/30.9.e36 (2002).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 


  • Source: Ecology - nature.com

    Crossing disciplines, adding fresh eyes to nuclear engineering

    Predicting building emissions across the US