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Eukaryote-Conserved Methylarginine Is Absent in Diplomonads and Functionally Compensated in Giardia

Emery-Corbin, Samantha J. (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.
Hamey, Joshua J. (author)
Univ New South Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW, Australia.
Ansell, Brendan R. E. (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.
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Balan, Balu (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.;Univ Melbourne, Fac Vet & Agr Sci, Melbourne Vet Sch, Dept Vet Biosci, Parkville, Vic, Australia.
Tichkule, Swapnil (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.
Stroehlein, Andreas J. (author)
Univ Melbourne, Fac Vet & Agr Sci, Melbourne Vet Sch, Dept Vet Biosci, Parkville, Vic, Australia.
Cooper, Crystal (author)
Queensland Univ Technol, Inst Future Environm, Cent Analyt Res Facil CARF, Brisbane, Qld, Australia.
McInerney, Bernie, V (author)
Macquarie Univ, Australian Proteome Anal Facil APAF, N Ryde, NSW, Australia.
Hediyeh-Zadeh, Soroor (author)
Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.;Walter & Eliza Hall Inst Med Res, Bioinformat Div, Parkville, Vic, Australia.
Vuong, Daniel (author)
Microbial Screening Technol, Smithfield, NSW, Australia.
Crombie, Andrew (author)
Microbial Screening Technol, Smithfield, NSW, Australia.
Lacey, Ernest (author)
Microbial Screening Technol, Smithfield, NSW, Australia.;Macquarie Univ, Fac Sci, Chem & Biomol Sci, N Ryde, NSW, Australia.
Davis, Melissa J. (author)
Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.;Walter & Eliza Hall Inst Med Res, Bioinformat Div, Parkville, Vic, Australia.
Wilkins, Marc R. (author)
Univ New South Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW, Australia.
Bahlo, Melanie (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.
Svärd, Staffan (author)
Uppsala universitet,Mikrobiologi
Gasser, Robin B. (author)
Univ Melbourne, Fac Vet & Agr Sci, Melbourne Vet Sch, Dept Vet Biosci, Parkville, Vic, Australia.
Jex, Aaron R. (author)
Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia.;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia.;Univ Melbourne, Fac Vet & Agr Sci, Melbourne Vet Sch, Dept Vet Biosci, Parkville, Vic, Australia.
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Walter & Eliza Hall Inst Med Res, Populat Hlth & Immun Div, Melbourne, Vic, Australia;Univ Melbourne, Dept Med Biol, Parkville, Vic, Australia. Univ New South Wales, Sch Biotechnol & Biomol Sci, Sydney, NSW, Australia. (creator_code:org_t)
2020-07-23
2020
English.
In: Molecular biology and evolution. - : OXFORD UNIV PRESS. - 0737-4038 .- 1537-1719. ; 37:12, s. 3525-3549
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  • Journal article (peer-reviewed)
Abstract Subject headings
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  • Methylation is a common posttranslational modification of arginine and lysine in eukaryotic proteins. Methylproteomes are best characterized for higher eukaryotes, where they are functionally expanded and evolved complex regulation. However, this is not the case for protist species evolved from the earliest eukaryotic lineages. Here, we integrated bioinformatic, proteomic, and drug-screening data sets to comprehensively explore the methylproteome of Giardia duodenalis-a deeply branching parasitic protist. We demonstrate that Giardia and related diplomonads lack arginine-methyltransferases and have remodeled conserved RGG/RG motifs targeted by these enzymes. We also provide experimental evidence for methylarginine absence in proteomes of Giardia but readily detect methyllysine. We bioinformatically infer 11 lysine-methyltransferases in Giardia, including highly diverged Su(var)3-9, Enhancer-of-zeste and Trithorax proteins with reduced domain architectures, and novel annotations demonstrating conserved methyllysine regulation of eukaryotic elongation factor 1 alpha. Using mass spectrometry, we identifymore than 200methyllysine sites in Giardia, including in species-specific gene families involved in cytoskeletal regulation, enriched in coiled-coil features. Finally, we use known methylation inhibitors to show that methylation plays key roles in replication and cyst formation in this parasite. This study highlights reduced methylation enzymes, sites, and functions early in eukaryote evolution, including absent methylarginine networks in the Diplomonadida. These results challenge the view that arginine methylation is eukaryote conserved and demonstrate that functional compensation of methylarginine was possible preceding expansion and diversification of these key networks in higher eukaryotes.

Subject headings

NATURVETENSKAP  -- Biologi -- Evolutionsbiologi (hsv//swe)
NATURAL SCIENCES  -- Biological Sciences -- Evolutionary Biology (hsv//eng)
NATURVETENSKAP  -- Biologi -- Biokemi och molekylärbiologi (hsv//swe)
NATURAL SCIENCES  -- Biological Sciences -- Biochemistry and Molecular Biology (hsv//eng)

Keyword

methylproteome
methylarginine
methyllysine
Diplomonadida
Metamonada
Giardia

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