Department of Biochemistry and Molecular Biology

Dalhousie University
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Michael W. Gray

Professor Emeritus

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Department of Biochemistry and Molecular Biology

Email: m.w.gray@dal.ca
Phone: 902-494-2521
Mailing Address: 
5850 College Street, Room 9-T2
Sir Charles Tupper Medical Building
PO Box 15000
Halifax, Nova Scotia, Canada B3H 4R2
 

Education

  • PhD, University of Alberta
  • FRSC

Academic Positions

  • Department member since 1970
  • Head of Department 2004-2007

Research Topics:

Protist Genomics, Mitochondria, Ribosomes

Research

Mitochondria and Ribosomes: Structure, Function and Evolution

For over four decades, my research program has centered on the origin and evolution of mitochondria and ribosomes, two complex subcellular structures in eukaryotic (nucleus-containing) cells. My group has explored gene evolution in mitochondrial and nuclear DNA of protists (mostly unicellular eukaryotes), and investigated the biochemistry of unique aspects of gene expression in mitochondria, such as RNA editing. Additionally, we have investigated naturally fragmented rRNAs that result from extensive and novel processing of rRNA precursors. The latter project also focused on small nucleolar RNAs (snoRNAs), which mediate post-transcriptional modification, such as ribose methylation and pseudouridine formation, in rRNA.

Protist Genomics

Currently, I am involved in the analysis and annotation of genome data generated from several different genome sequencing projects focused on protists, including two amoebozoons, Acanthamoeba castellanii and Physarum polycephalum, two nucleomorph-containing algae, Bigelowiella natans and Guillardia theta, and a number of eukaryotic microbes (protists and fungi) selected to explore the origins of multicellularity in animals and fungi (http://www.broadinstitute.org/annotation/genome/multicellularity_project/MultiHome.html).

Keywords:

mitochondria; ribosomes; snoRNA; RNA editing; protists; genomics

Publications

  1. Horvathova, L., Žarsky, V., Panek, T., Derelle, R., Pyrih, J., Motyčkova, A., Klapšťova, V., Klimeš, V., Petrů, M., Vaitova, Z., Čepička, I., Harant, K., Gray, M.W., Guilvout, I., Francetic, O., Lang, B.F., Vlček, C., Tsaousis, A.D., Eliaš, M., and Doležal, P. (2021) Analysis of diverse eukaryotes suggests the existence of an ancestral mitochondrial apparatus derived from the bacterial type II secretion system. Nat. Commun. 12, 2947 [PubMed] [Article]
  2. Gray, M.W. and Gopalan, V. (2020) Piece by piece: the making of a ribozyme. J. Biol. Chem. 295:2313-2323 [PubMed] [Article]
  3. Matzov, D., Taoka, M., Nobe, Y., Yamauchi, Y., Halfon, Y., Asis, N., Zimmermann, E., Rozenberg, H., Bashan, A., Bhushan, S., Isobe, T., Gray, M.W., Yonath, A. and Shalev-Benami, M. (2020) Cryo-EM structure of the highly atypical cytoplasmic ribosome of Euglena gracilis. Nucleic Acids Res. 4811750-11761 [PubMed] [Article]
  4. Valach, M., Gonzalez Alcazar, J.A., Sarrasin, M., Lang, B. F., Gray, M.W., and Burger, G. (2020) An unexpectedly complex mitoribosome in Andalucia godoyi, a protist with the most bacteria-like mitochondrial genome. Mol. Biol. Evol. 38:788-804 [PubMed] [Article]
  5. Gray, M.W., Burger, G, Derelle, R., Klimeš, V., Leger, M., Sarrasin, M.,Vlček, C., Roger, A. J., Eliáš, M. and Lang, B.F. (2020) The draft nuclear genome sequence and predicted mitochondrial proteome of Andalucia godoyi, a protist with the most gene-rich and bacteria-like mitochondrial genome. BMC Biol. 18:22 [PubMed] [Article]
  6. Dodbele, S., Jackman, J.E., and Gray, M.W., (2018) Mechanisms and evolution of mitochondrial tRNA 5′-editing In RNA Metabolism in Mitochondria (Cruz-Reyes, J. and Gray, M.W., eds.) Vol. 34, Nucleic Acids and Molecular Biology, Springer International Publishing AG:177-198
  7. Gray, M.W. and Mootha, V.K., (2018) Evolutionary mitochondrial biology in Titisee IUBMB Life 70:1184-1187 [PubMed] [Article]
  8. Valach, M., Léveillé-Kunst, A., Gray, M.W., and Burger, G., (2018) Respiratory chain Complex I: subunits of unparalelled divergence in diplonemids J. Biol. Chem. 293:16043-16056 [PubMed] [Article]
  9. Gray, M.W., (2017) Lynn Margulis and the endosymbiont hypothesis: 50 years later. Mol. Biol. Cell 28:1285-1287 [PubMed] [Article]
  10. Gray, M.W., (2015) The mosaic nature of the mitochondrial proteome: implications for the origin and evolution of mitochondria. Proc. Natl. Acad. Sci. U.S.A. 112:10133-10138 [PubMed] [Article]
  11. David, V., Flegontov, P., Gerasimov, E.,Tanifuji, G.,Hashimi, H., Logacheva, M.G., Maruyama, S., Onodera, N.T., Gray, M.W., Archibald, J.M. and Lukeš, J., (2015) Gene loss and error-prone RNA editing in the mitochondrion of Perkinsela, an endosymbiotic kinetoplastid. mBio 6:e01498-15
  12. Gray, M.W., (2014) Organelle evolution, fragmented ribosomal RNAs, and Carl. RNA Biol. 11:213-216 [PubMed] [Article]
  13. Abad, M.G., Long, Y., Kinchen, D., Schindel, E.T., Gray, M.W. and Jackman, J.E., (2014) Mitochondrial tRNA 5′-editing in Dictyostelium discoideum and Polysphondylium pallidum. J. Biol. Chem. 289:15155-15165 [PubMed] [Article]
  14. Gawryluk, R.M.R., Chisholm, K.A., Pinto, D.M. and Gray, M.W., (2014) Compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa) rivals that of animals, fungi, and plants. J. Proteomics 109:400-416 [PubMed] [Article]
  15. Gawryluk, R.M.R., Chisholm, K.A., Pinto, D.M. and Gray, M.W., (2014) Data showing the compositional complexity of the mitochondrial proteome of a unicellular eukaryote (Acanthamoeba castellanii, supergroup Amoebozoa). Data in Brief 1:12-14
  16. Valach, M., Burger, G., Gray, M.W. and Lang, B.F., (2014) Widespread occurrence of mitochondrial genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res. 42:13764-13777 [PubMed] [Article]
  17. Gray, M.W., (2013) The pre-endosymbiont hypothesis: a new perspective on the origin and evolution of mitochondria. Cold Spring Harb. Perspect. Biol. 6: a016097 [PubMed]
  18. Rao, B.S., Mohammad, F., Gray, M.W. and Jackman, J.E. , (2013) Absence of a universal element for tRNAHis identity in Acanthamoeba castellanii. Nucleic Acids Res. 41:1885-1894 [PubMed]
  19. Li, L., Nelson, C.J., Carrie, C., Gawryluk, R.M.R., Solheim, C., Gray, M.W., Whelan, J. and Millar, A.H., (2013) Subcomplexes of ancestral respiratory complex I subunits rapidly turn over in vivo as productive assembly intermediates in Arabidopsis. J. Biol. Chem. 288:5707-5717 [PubMed]
  20. Gray, M. W., (2013) Mitochondrial genomes. Molecular Life Sciences: An Encyclopedic Reference, E. Bell, J. S. Bond, J. P. Klinman, B. S. S. Masters and R. D. Wells (eds.), Springer:DOI: 10.1007/SpringerReference_333640 2014-03-20 13:49:09 UTC
  21. Burger, G., Gray, M.W., Forget, L. and Lang, B.F., (2013) Strikingly bacteria-like and gene-rich mitochondrial genomes throughout jakobid protists. Genome Biol. Evol. 5:418-438 [PubMed]
  22. Gray, M.W., (2013) RNA editing: evolutionary implications. eLS 2013 John Wiley & Sons, Ltd., Chichester: DOI: 10.1002/9780470015902.a0003069.pub3
  23. Leger, M.M., Gawryluk, R.M.R., Gray, M.W. and Roger, A.J. , (2013) Evidence for a hydrogenosomal-type ATP generation system in Acanthamoeba castellanii. PLoS One 8:e69532 [PubMed] [Article]
  24. Wideman, J.G., Gawryluk, R.M.R., Gray, M.W. and Dacks, J.B., (2013) The ancient and widespread nature of the ER-Mitochondria Encounter Structure. Mol. Biol. Evol. 30:2044-2049 [PubMed]
  25. Pombert J.-F., Smirnov, A, James, E.R., Janouškovec, J., Gray, M.W. and Keeling, P.J., (2013) The complete mitochondrial genome from an unidentified Phalansterium species. Protist Genomics 1:26-32 [Article]
  26. Gray, M.W., (2012) Organelles. Brenner's Online Encyclopedia of Genetics 2E, S. Maloy and K. Hughes (eds.), Academic Press: in press
  27. Gray, M.W., (2012) Mitochondria. Brenner's Online Encyclopedia of Genetics 2E, S. Maloy and K. Hughes (eds.), Academic Press: in press
  28. Gray, M.W., (2012) Mitochondrial DNA. Brenner's Online Encyclopedia of Genetics 2E, S. Maloy and K. Hughes (eds.), Academic Press : in press
  29. Gray, M.W., (2012) Mitochondrial genome. Brenner's Online Encyclopedia of Genetics 2E, S. Maloy and K. Hughes (eds.), Academic Press : in press
  30. Gray, M.W., (2012) Mitochondrial mutants. Brenner's Online Encyclopedia of Genetics 2E, S. Maloy and K. Hughes (eds.), Academic Press : in press
  31. Gray, M.W. and Archibald, J.M., (2012) Origins of mitochondria and plastids. Genomics of Chloroplasts and Mitochondria, R. Bock and V. Knoop (eds.) Springer, Dordrecht:1-30
  32. Jackman, J.E., Gott, J.M. and Gray, M.W., (2012) Doing it in reverse: 3′-to-5′ polymerization by the Thg1 superfamily. RNA 18:886-899 [PubMed]
  33. Gray, M.W., (2012) Mitochondrial evolution Cold Spring Harb Perspect Biol 4:a011403 [PubMed]
  34. Gawryluk, R.M.R., Chisholm, K.A., Pinto, D.M. and Gray, M.W., (2012) Composition of the mitochondrial electron transport chain in Acanthamoeba castellanii: structural and evolutionary insights Biochim. Biophys. Acta 1817:2027-2037 [PubMed]
  35. Gray, M.W., (2012) Evolutionary origin of RNA editing. Biochemistry 51:5235-5242 [PubMed]
  36. Hopkins, J. F., Spencer, D. F., Laboissiere, S., Neilson, J. A. D., Eveleigh, R. J. M., Durnford, D. G., Gray, M. W. and Archibald, J. M., (2012) Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol. Evol. 4:1391-1405 [PubMed]
  37. Gray, M.W., (2011) The incredible shrinking organelle. EMBO Rep. 12:873 [PubMed]
  38. Gray, M.W. and Beyer, A.L, (2011) Ribonucleic acid (RNA). McGraw Hill Encyclopedia of Science & Technology, 11th edition : in press
  39. Spencer, D.F. and Gray, M.W., (2011) Ribosomal RNA genes in Euglena gracilis mitochondrial DNA: fragmented genes in a seemingly fragmented genome. Mol. Genet. Genomics 285:19-31 [PubMed]
  40. Abad, M.G., Long, Y., Willcox, A., Gott, J.M., Gray, M.W. and Jackman, J.E., (2011) A role for tRNAHis guanylyltransferase (Thg1)-like proteins from Dictyostelium discoideum in mitochondrial 5′-tRNA editing. RNA 17:613-623 [PubMed]
  41. Doolittle, W.F., Lukeš, J., Archibald, J.M.. Keeling, P.J. and Gray, M.W., (2011) Comment on “Does constructive neutral evolution play an important role in the origin of cellular complexity?” Bioessays 33:427-429 [PubMed]
  42. Lukeš, J., Archibald, J.M., Keeling, P.J., Doolittle, W.F. and Gray, M.W. , (2011) How a neutral evolutionary ratchet can build cellular complexity. IUBMB Life 63:528-537 [PubMed]
  43. Flegontov, P., Gray, M.W., Burger, G. and Lukeš, J., (2011) Gene fragmentation: a key to mitochondrial genome evolution in Euglenozoa? Curr. Genet. 57:225-232 [PubMed]
  44. Schnare, M.N. and Gray, M.W., (2011) Complete modification maps for the small and large subunit rRNAs of Euglena gracilis: functional and evolutionary implications of contrasting patterns between the two rRNA components J. Mol. Biol. 413:66-83 [PubMed]
  45. Gray, M.W., (2010) Re-thinking plastid evolution. EMBO Rep 11:562-563 [PubMed]
  46. Gawryluk, R.M.R. and Gray, M.W., (2010) Evidence for an early evolutionary emergence of γ-type carbonic anhydrases as components of mitochondrial respiratory complex I. BMC Evol. Biol. 10:176 [PubMed]
  47. Gawryluk, R.M.R. and Gray, M.W., (2010) An ancient fission of mitochondrial cox1. Mol. Biol. Evol. 27:7-10 [PubMed]
  48. Gott, J.M., Somerlot, B.H. and Gray, M.W., (2010) Two forms of RNA editing are required for tRNA maturation in Physarum mitochondria. RNA 16:482-488 [PubMed]
  49. Bullerwell, C.E., Burger, G., Gott, J.M., Kourennaia, O., Schnare, M.N. and Gray, M.W., (2010) Abundant 5S rRNA-like transcripts encoded by the mitochondrial genome in Amoebozoa. Eukaryot. Cell 9:762-773 [PubMed]
  50. Gray, M.W., Lukeš, J., Archibald, J.M., Keeling, P.J. and Doolittle, W.F., (2010) Irremediable complexity? Science 330:920-921 [PubMed]
  51. Gray, M.W., (2009) RNA editing in plant mitochondria: 20 years later. IUBMB Life 61:1101-1104 [PubMed]
  52. Gawryluk, R.M.R. and Gray, M.W., (2009) A split and rearranged nuclear gene encoding the iron-sulfur subunit of mitochondrial succinate dehydrogenase in Euglenozoa. BMC Res. Notes 2:16 [PubMed]
  53. Gray, M.W., (2009) The path to RNA editing in plant mitochondria: the Halifax chapter. IUBMB Life 61:1114-1117 [PubMed]
  54. Charette, J.M. and Gray, M.W. , (2009) U3 snoRNA genes are multi-copy and frequently linked to U5 snRNA genes in Euglena gracilis. BMC Genomics 10:528 [PubMed]
  55. Watkins, R.F. and Gray, M.W., (2008) Sampling gene diversity across the supergroup Amoebozoa: large EST data sets from Acanthamoeba castellanii, Hartmannella vermiformis, Physarum polycephalum, Hyperamoeba dachnaya and Hyperamoeba sp. Protist 159:269-281 [PubMed]
  56. Lin, S., Zhang, H. and Gray, M.W., (2008) RNA editing in dinoflagellates and its implications for the evolutionary history of the editing machinery. In RNA and DNA Editing: Molecular Mechanisms and Their Integration into Biological Systems (Smith, H.C., ed.) Wiley Press:280-309
  57. Ruiz-Trillo, I., Roger, A.J., Burger, G., Gray, M.W. and Lang, B.F., (2008) A phylogenomic investigation into the origin of Metazoa. Mol. Biol. Evol. 25:664-672 [PubMed]
  58. O'Brien, E.A., Koski, L.B., Zhang, Y., Yang, L., Wang, E., Gray, M.W., Burger, G. and Lang, B.F., (2007) TBestDB: a taxonomically broad database of expressed sequence tags (ESTs). Nucleic Acids Res. 35:D445-D451 [PubMed]
  59. Ruiz-Trillo, I., Burger, G., Holland, P.W.H., King, N., Lang, B.F., Roger, A.J. and Gray, M.W., (2007) The origins of multicellularity: a multi-taxon genome initiative. Trends Genet. 23:113-118 [PubMed]
  60. Lohan, A.J. and Gray, M.W., (2007) Analysis of 5'- or 3'-terminal tRNA editing: mitochondrial 5' editing in Acanthamoeba castellanii as the exemplar. Methods Enzymol. 424: 221-242 [PubMed]
  61. Rogers, M.B., Watkins, R.F., Harper, J.T., Durnford, D.G., Gray, M.W. and Keeling, P.J., (2007) A complex and punctate distribution of three eukaryotic genes derived by lateral gene transfer. BMC Evol. Biol. 7: 89 [PubMed]
  62. Rodríguez-Ezpeleta, N., Brinkmann, H., Burger, G., Roger, A. J., Gray, M.W., Philippe, H. and Lang, B.F., (2007) Towards resolving the eukaryotic tree: the phylogenetic positions of jakobiods and cercozoans. Curr. Biol. 17:1420-1425 [PubMed]
  63. Jackson, C. J., Norman, J. E., Schnare, M. N., Gray, M. W., Keeling, P. J. and Waller, R. F., (2007) Broad genomic and transcriptional analysis reveals a highly derived genome in dinoflagellate mitochondria. BMC Biol. 5: 41 [PubMed]
  64. Smith, D. G. S., Gawryluk, R. M. R., Spencer, D. F., Pearlman, R. E., Siu, K. W. M. and Gray, M. W., (2007) Exploring the mitochondrial proteome of the ciliate protozoon, Tetrahymena thermophila: direct analysis by tandem mass spectrometry. J. Mol. Biol. 374: 837-863 [PubMed]
  65. Shutt, T.E. and Gray, M.W., (2006) Twinkle, the mitochondrial replicative DNA helicase, is widespread in the eukaryotic radiation and may also be the mitochondrial DNA primase in most eukaryotes. J. Mol. Evol. 62:588-599 [PubMed]
  66. Durnford, D.G. and Gray, M.W., (2006) Analysis of Euglena gracilis plastid-targeted proteins reveals different classes of transit sequences. Eukaryot. Cell 5:2079-2091 [PubMed]
  67. Shutt, T.E. and Gray, M.W. , (2006) Bacteriophage origins of mitochondrial replication and transcription proteins. Trends Genet. 22:90-95 [PubMed]
  68. Russell, A.G., Schnare, M.N. and Gray, M.W., (2006) A large collection of compact box C/D snoRNAs and their isoforms in Euglena gracilis: structural, functional and evolutionary insights. J. Mol. Biol. 357: 1548-1565 [PubMed]
  69. Shutt, T.E. and Gray, M.W., (2006) Homologs of mitochondrial transcription factor B, sparsely distributed within the eukaryotic radiation, are likely derived from the dimethyladenosine methyltransferase of the mitochondrial endosymbiont. Mol. Biol. Evol. 23:1169-1179 [PubMed]
  70. Watkins, R.F. and Gray, M.W., (2006) The frequency of eubacterium-to-eukaryote lateral gene transfers shows significant cross-taxa variation in the phylum Amoebozoa. J. Mol. Evol. 63:801-814 [PubMed]
  71. Russell, A.G., Charette, J.M., Spencer, D.F. and Gray, M.W. , (2006) An early evolutionary origin for the minor spliceosome. Nature 443:863-866 [PubMed]
  72. Bullerwell, C.E. and Gray, M.W., (2005) In vitro characterization of a tRNA editing activity in the mitochondria of Spizellomyces punctatus, a chytridiomycete fungus. J. Biol. Chem. 280:2463-2470 [PubMed]
  73. Gray, M.W., (2005) Contemporary issues in mitochondrial origins and evolution. Microbial Phylogeny and Evolution (J. Sapp, ed.) Oxford University Press, New York:224-237
  74. Gray, M. W., (2005) The hydrogenosome's murky past. Nature 434:29-31 [PubMed]
  75. Anderson, I.J., Watkins, R.F., Samuelson, J., Spencer, D.F., Majoros, W.H., Gray, M.W. and Loftus, B.J., (2005) Gene discovery in the Acanthamoeba castellanii genome. Protist 156:203-214 [PubMed]
  76. Russell, A.G., Watanabe, Y-i., Charette, J.M. and Gray, M.W., (2005) Unusual features of fibrillarin cDNA and gene structure in Euglena gracilis: evolutionary conservation of core proteins in methylation-guide box C/D snoRNPs throughout the domain Eucarya. Nucleic Acids Res. 33:2781-2791 [PubMed]
  77. Koski, L.B., Gray, M.W., Lang, B.F. and Burger, G., (2005) AutoFACT: an Automatic Functional Annotation and Classification Tool. BMC Bioinfomatics 6:151 [PubMed]
  78. Keeling, P.J., Burger, G., Durnford, D.G., Lang, B.F., Lee, R.W., Pearlman, R.E., Roger, A. J. and Gray, M.W. , (2005) The tree of eukaryotes. Trends Ecol. Evol. 20: 670-676 [PubMed]
  79. Russell, A.G., Shutt, T.E., Watkins, R.F. and Gray, M.W., (2005) An ancient spliceosomal intron in the ribosomal protein L7a gene (Rpl7a) of Giardia lamblia. BMC Evol. Biol. 5:45 [PubMed]