- Canada Research Chair (Tier II) in Evolutionary Cell Biology, 2011-2021
- 2016 Hutner Award (presented by the International Society of Protistologists)
The membrane-trafficking system is a key characteristic of eukaryotes (humans, plants, yeast, etc.) and one of the defining features that separates us from bacteria at a cellular level. It is responsible for the proper movement and final location of most of the material in our cells. It underlies not only brain activity, and hormone secretion in humans, but healthy plant growth, as well as normal cellular activity in a diverse array of single-celled organisms important for our economy, our environment and our health. The pathogenic mechanisms of many parasites, such as the organisms causing malaria, primary amoebic meningoencephalitis and African sleeping sickness, are all underpinned by action of the membrane-trafficking system.
Evidence suggests that the membrane-trafficking system arose early on in eukaryotic evolution, with the major protein families involved likely having been already present in our ancestors over one billion years ago. The innovation of an endomembrane system would have been crucial for early eukaryotes, allowing predation, surface remodelling and increased cell size.
The long-term goal of my research program is to understand the evolution and diversity of the eukaryotic membrane-trafficking system.
Although evolutionary in nature, my research also provides insight into basic cell biology, parasitism and pathogenesis. By comparative genomics and evolutionary cell biology addressing organisms from across the taxonomic breadth of eukaryotes (beyond yeast to man), core components of eukaryotic cellular systems are identified. This allows the development of models of cell biological mechanism that are valid for all eukaryotic cells. It is also possible to place in context some aspects that are unique to a particular model system. Features that are unique, when found in parasitic protistan pathogens, may represent potential therapeutic targets.
We use genomics and molecular evolutionary tools such as phylogenetics and homology searching to address our questions. Some of our analyses involve searching publicly available genome data. Additionally, the lab participates in international sequencing projects of protist genomes to examine their membrane trafficking machinery. This has included important microbial parasites (eg. Trichomonas vaginalis, Blastocystis hominis, and on-going work for Naegleria fowleri), as well as important free-living relatives of parasites (eg. Bodo saltans, Euglena gracilis, Naegleria gruberiand Chromera velia/Vitrella brassicaformis). We are also interested in protists of ecological and evolutionary importance (eg. Emiliania huxleyi, Guillardia theta, Bigelowiella natans, Monocercomonoides exilis).
Several interconnected lines of research are currently on-going in my lab relating ancient origins of the endomembrane system and the subsequent evolution in modern eukaryotes:
Origin and evolution of the membrane trafficking system Detailed evolutionary studies of individual protein families (eg. SNAREs, vesicle coats) can reveal important information about the specific history of that membrane-trafficking machinery and about the membrane-trafficking system in general. Such studies have thus far demonstrated ancient complexity in the trafficking system and the proposal of an evolutionary mechanism for non-endosymbiotic organelle evolution. As a by-product of these investigations, we have uncovered new protein complexes and trafficking pathways, even in human cells and revealed the cryptic origin of others relevant to neurodegenerative diseases. We continue to investigate the evolution of protein families involved in membrane-trafficking, with the goal of understanding the emergence of specificity and organelle identity in the eukaryotic cell.
While some membrane trafficking organelles are conserved across eukaryotes, poorly understood organelles are present outside the well -known model systems that are ripe for exploration. The Contractile Vacuole (CV) is an osmoregulatory organelle found in ecologically important freshwater and soil-dwelling organisms. However, it is often not reported as present in parasites or marine organisms, raising questions of whether organelles identified as contractile vacuoles are truly orthologous between diverse eukaryotes. We have an NSERC-funded research program to use molecular evolutionary and transcriptomic analysis to examine the evolution and function of the CV across the breadth of protist lineages.
Evolutionary parasitology and Global Health Some of the world’s most significant infectious diseases are caused by microbial eukaryotes. Our work investigates the ways in which the cell biology of membrane-trafficking, as we understand it primarily from studies in animal and yeast models, applies to that of organisms that cause significant mortality and poverty across the world. We often collaboratively pair our in silico work with molecular cell biology to test hypotheses. Current work includes the evolution of invasion organelles in Apicomplexa (malaria, toxoplasmosis) and of non-canonical organelles (eg. Peripheral Vacuoles) in the Fornicata (eg. Giardia, the organism causing Beaver Fever). We are also among research groups leading the genome sequencing project of Naegleria fowleri (the brain-eating amoeba).
Furthermore, I am the co-founder and co-director of the (UAlberta) Biomedical Global Health Research Network. The goal of the network is to facilitate interaction between UAlberta researchers doing biomedical work with relevance to, and in aid of, Global Health.
Additional research lines include microbial eukaryotes in oilsands-associated environmentsand genomics of microbial eukaryotesto better understand the diversity of membrane-trafficking machinery and the evolutionary processes that shape the endomembrane system in lineages post-LECA
amoeba, Bio-diversity, endocytosis, Environmental monitoring, Evolution, organelle, membrane-trafficking, genome, meningitis, Microbial eukaryotes, Naegleria, Next-Generation Sequencing, Systems Biology
Selected peer-reviewed publications (* denotes equal contribution, **denotes JBD as corresponding author, trainees underlined, visiting scientists underlined and italicized)
Origin and evolution of the membrane trafficking system
Ramirez-Macias I, BarlowLD, Anton C, Spang A, Roncero C, Dacks JB**. Evolutionary cell biology traces the rise of the exomer complex in Fungi from an ancient eukaryotic component. Sci Rep.2018 Jul 24;8(1):11154.
Barlow LD, Nývltová E, Aguilar M, Tachezy J, Dacks JB**.A sophisticated, differentiated Golgi in the ancestor of eukaryotes. BMC Biol.2018 Mar 7;16(1):27. 2016
Klinger CM*, Spang A*, Dacks JB**, Ettema TJG. Tracing the archaeal origins of eukaryotic membrane-trafficking system building blocks. Mol Biol Evol.(2016). Jun;33(6):1528-41.
Hirst J*, Schlacht A*, Norcott JP, Traynor D, Bloomfield G, Antrobus R, Kay RR, Dacks JB**,Robinson MS. Characterization of TSET, an ancient and widespread membrane trafficking complex. eLife.2014 May 27;3:e02866.
Schlacht A, Herman EK, Klute MJ, Field MC and Dacks JB**. Missing pieces of an ancient puzzle: Evolution of the eukaryotic membrane-trafficking system (2014) Cold Spring Harb Perspect Biol. 1;6(10). pii: a016048.
Elias M, Brighouse A, Gabernet-Castello C, Field MC, Dacks JB**. Sculpting the endomembrane system in deep time: high resolution phylogenetics of Rab GTPases. J Cell Sci. 2012 May 15;125(Pt 10):2500-8
Hirst J, Barlow LD, Francisco GC, Sahlender DA, Seaman MN, Dacks JB**, Robinson MS. The fifth adaptor protein complex. PLoS Biol.2011 Oct;9(10):e1001170.
Evolutionary parasitology and Global Health
Ebrahimzadeh Z, Mukherjee A, Crochetière M-E, Sergerie A, Amiar S,Thompson LA, Gagnon D, Gaumond D, Stahelin RV, Dacks JB, Richard D.A pan-apicomplexan phosphoinositide-binding protein acts in malarial microneme exocytosis. EMBO Reports 2019 May 16. pii: e47102
Herman E, Siegesmund MA, Bottery MJ, van Aerle R, Shather MM, Caler E, Dacks JB**, van derGiezen M. Membrane Trafficking Modulation during Entamoeba Encystation. Sci Rep.2017 Oct 9;7(1):12854
Venkatesh D, Boehm C, Barlow LD, Nankissoor NN, O'Reilly A, Kelly S, Dacks JB, Field MC. Evolution of the endomembrane systems of trypanosomatids - conservation and specialisation. J Cell Sci. 2017 Apr 15;130(8):1421-1434.
Klinger CM, Macias I, Herman EK, Turkewitz A, Field MC, and Dacks JB**. Testing the assumption of functional homology in the membrane-trafficking system, a perspective from model parasites. Mol. Biochem Parasitol(2016). Sep - Oct;209(1-2):88-103.
Klinger CM, Klute MJ, Dacks JB**. Comparative Genomic Analysis of Multi-subunit Tethering Complexes Demonstrates an Ancient Pan-Eukaryotic Complement and Sculpting in Apicomplexa.PLoS One.2013 Sep 27;8(9):e76278
Microbial Eukaryotic Genomics (parasitology related)
Ebenezer TE, Zoltner M, Burrell A, Nenarokova A, Novák Vanclová AMG, Prasad B, Soukal P, Santana-Molina C, O'Neill E, Nankissoor NN, Vadakedath N, Daiker V, Obado S, Silva-Pereira S, Jackson AP, Devos DP, Lukeš J, Lebert M, Vaughan S,Hampl V, Carrington M, Ginger ML, Dacks JB**, Kelly S, Field MC. Transcriptome, proteome and draft genome of Euglena gracilis. BMC Biol. 2019 Feb 7;17(1):11.
Gentekaki E, Curtis BA, Stairs CW, Klimeš V, Eliáš M, Salas-Leiva DE, HermanEK, Eme L, Arias MC, Henrissat B, Hilliou F, Klute MJ, Suga H, Malik SB, Pightling AW, Kolisko M, Rachubinski RA, Schlacht A, Soanes DM, Tsaousis AD, Archibald JM, Ball SG, Dacks JB, Clark CG, van der Giezen M, Roger AJ. Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis.PLoS Biol.2017 Sep 11;15(9):e2003769.
Jackson AP, Otto TD, Aslett M, Armstrong SD, Bringaud F, Schlacht A, Hartley C, Sanders M, Wastling JM, Dacks JB, Acosta-Serrano A, Field MC, Ginger ML, Berriman M. Kinetoplastid Phylogenomics Reveals the Evolutionary Innovations Associated with the Origins of Parasitism. Curr Biol.2016 Jan 25;26(2):161-72.
Woo YH, Ansari H, Otto TD, Klinger CM, Kolisko M, Michálek J, Saxena A, Shanmugam D, Tayyrov A, Veluchamy A, Ali S, Bernal A, Del Campo J, Cihlář J, Flegontov P, Gornik SG, Hajdušková E, Horák A, Janouškovec J, Katris NJ, Mast FD, Miranda-Saavedra D, Mourier T, Naeem R, Nair M, Panigrahi AK, Rawlings ND, Padron-Regalado E, Ramaprasad A, Samad N, Tomčala A, Wilkes J, Neafsey DE, Doerig C, Bowler C, Keeling PJ, Roos DS, Dacks JB, Templeton TJ, Waller RF, Lukeš J, Oborník M, Pain A. Chromerid genomes reveal the evolutionary path from photosynthetic algae to obligate intracellular parasites. eLife.2015 Jul 15;4:e06974.
Microbial eukaryotes in oilsands-associated environments and genomics of microbial eukaryotes
Aguilar M, Richardson E,TanB, Walker G, Dunfield P, BassD, Nesbø C, Foght J, Dacks JB**. Next-generation Sequencing Assessment of Eukaryotic Diversity in Oil Sands Tailings Ponds Sediments and Surface Water J. Euk Micro. (2016) Nov;63(6):732-743.
Karnkowska A, Vacek V, Zubáčová Z, Treitli, S C, Petrželková R, Eme L, Novák L, Žárský V, Barlow LD, Herman EK, Soukal P, Hroudová M, Doležal P, Stairs CW, Roger AJ, Eliáš M, Dacks JB, Vlček Č and Hampl V. A eukaryote without a mitochondrial organelle Curr. Biol. (2016)May 23;26(10):1274
Read BA, Kegel J, Klute MJ, Kuo A, Lefebvre SC, Maumus F, Mayer C, Miller J, Monier A, Salamov A, Young J, Aguilar M, Claverie JM, Frickenhaus S, Gonzalez K, Herman EK, Lin YC, Napier J, Ogata H, Sarno AF, Shmutz J, Schroeder D, de Vargas C, Verret F, von Dassow P, Valentin K, Van de Peer Y, Wheeler G; Emiliania huxleyi Annotation Consortium, Dacks JB*, Delwiche CF*, Dyhrman ST*, Glöckner G*, John U*, Richards T*, Worden AZ*, Zhang X*, Grigoriev IV. Pan genome of the phytoplankton Emiliania underpins its global distribution. Nature.2013 Jul 11;499(7457):209-13.
Curtis BA, Tanifuji G, Burki F, Gruber A, Irimia M, Maruyama S, Arias MC, Ball SG, Gile GH, Hirakawa Y, Hopkins JF, Kuo A, Rensing SA, Schmutz J, Symeonidi A, Elias M, Eveleigh RJ, Herman EK, Klute MJ, Nakayama T, Oborník M, Reyes-Prieto A, Armbrust EV, Aves SJ, Beiko RG, Coutinho P, Dacks JB, Durnford DG, Fast NM, Green BR, Grisdale CJ, Hempel F, Henrissat B, Höppner MP, Ishida K, Kim E, Kořený L, Kroth PG, Liu Y, Malik SB, Maier UG, McRose D, Mock T, Neilson JA, Onodera NT, Poole AM, Pritham EJ, Richards TA, Rocap G, Roy SW, Sarai C, Schaack S, Shirato S, Slamovits CH, Spencer DF, Suzuki S, Worden AZ, Zauner S, Barry K, Bell C, Bharti AK, Crow JA, Grimwood J, Kramer R, Lindquist E, Lucas S, Salamov A, McFadden GI, Lane CE, Keeling PJ, Gray MW, Grigoriev IV, Archibald JM. Algal genomes reveal evolutionary mosaicism and the fate of nucleomorphs. Nature.2012 Dec 6;492(7427):59-65.