Most trypanosomatid flagellates do not have catalase. In the evolution of this group, the gene encoding catalase has been independently acquired at least three times from three different bacterial groups. Here, we demonstrate that the catalase of Vickermania was obtained by horizontal gene transfer from Gammaproteobacteria, extending the list of known bacterial sources of this gene. Comparative biochemical analyses revealed that the enzymes of V. ingenoplastis, Leptomonas pyrrhocoris, and Blastocrithidia sp., representing the three independent catalase-bearing trypanosomatid lineages, have similar properties, except for the unique cyanide resistance in the catalase of the latter species.

Life Science Research Centre Faculty of Science University of Ostrava 71000 Ostrava Czech Republic

Martsinovsky Institute of Medical Parasitology Tropical and Vector Borne Diseases Sechenov University 119435 Moscow Russia

Nuffield Department of Medicine University of Oxford Old Road Campus Headington Oxford OX3 7BN UK

Zoological Institute of the Russian Academy of Sciences 199034 St Petersburg Russia

Zobrazit více v PubMed

Zámocký M., Furtmüller P.G., Obinger C. Evolution of catalases from bacteria to humans. Antioxid. Redox Signal. 2008;10:1527–1548. doi: 10.1089/ars.2008.2046. PubMed DOI PMC

Zámocký M., Koller F. Understanding the structure and function of catalases: Clues from molecular evolution and in vitro mutagenesis. Prog. Biophys. Mol. Biol. 1999;72:19–66. doi: 10.1016/S0079-6107(98)00058-3. PubMed DOI

Nicholls P., Fita I., Loewen P.C. Enzymology and structure of catalases. Adv. Inorg. Chem. 2000;51:51–106.

Glorieux C., Calderon P.B. Catalase, a remarkable enzyme: Targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biol. Chem. 2017;398:1095–1108. doi: 10.1515/hsz-2017-0131. PubMed DOI

Alfonso-Prieto M., Biarnés X., Vidossich P., Rovira C. The molecular mechanism of the catalase reaction. J. Am. Chem. Soc. 2009;131:11751–11761. doi: 10.1021/ja9018572. PubMed DOI

Sies H., Jones D.P. Reactive oxygen species (ROS) as pleiotropic physiological signalling agents. Nat. Rev. Mol. Cell Biol. 2020;21:363–383. doi: 10.1038/s41580-020-0230-3. PubMed DOI

Halliwell B. Antioxidant defence mechanisms: From the beginning to the end (of the beginning) Free Radic. Res. 1999;31:261–272. doi: 10.1080/10715769900300841. PubMed DOI

Loew O. Catalase, a New Enzym of General Occurrence, with Special Reference to the Tobacco Plant. Volume 68. Goverment Printing Office; Washington, DC, USA: 1901. p. 44. US Department of Africulture Reports.

Murthy M.R., Reid T.J., 3rd, Sicignano A., Tanaka N., Rossmann M.G. Structure of beef liver catalase. J. Mol. Biol. 1981;152:465–499. doi: 10.1016/0022-2836(81)90254-0. PubMed DOI

Vainshtein B.K., Melik-Adamyan W.R., Barynin V.V., Vagin A.A., Grebenko A.I. Three-dimensional structure of the enzyme catalase. Nature. 1981;293:411–412. doi: 10.1038/293411a0. PubMed DOI

Maté M.J., Zámocký M., Nykyri L.M., Herzog C., Alzari P.M., Betzel C., Koller F., Fita I. Structure of catalase—A from Saccharomyces cerevisiae. J. Mol. Biol. 1999;286:135–149. PubMed

Faguy D.M., Doolittle W.F. Horizontal transfer of catalase-peroxidase genes between archaea and pathogenic bacteria. Trends Genet. 2000;16:196–197. doi: 10.1016/S0168-9525(00)02007-2. PubMed DOI

Škodová-Sveráková I., Záhonová K., Bučková B., Füssy Z., Yurchenko V., Lukeš J. Catalase and ascorbate peroxidase in euglenozoan protists. Pathogens. 2020;9:317. PubMed PMC

Kraeva N., Horáková E., Kostygov A., Kořený L., Butenko A., Yurchenko V., Lukeš J. Catalase in Leishmaniinae: With me or against me? Infect. Genet. Evol. 2017;50:121–127. doi: 10.1016/j.meegid.2016.06.054. PubMed DOI

Keeling P.J., Palmer J.D. Horizontal gene transfer in eukaryotic evolution. Nat. Rev. Genet. 2008;9:605–618. doi: 10.1038/nrg2386. PubMed DOI

Husnik F., McCutcheon J.P. Functional horizontal gene transfer from bacteria to eukaryotes. Nat. Rev. MicroBiol. 2018;16:67–79. doi: 10.1038/nrmicro.2017.137. PubMed DOI

Thomas C.M., Nielsen K.M. Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat. Rev. MicroBiol. 2005;3:711–721. doi: 10.1038/nrmicro1234. PubMed DOI

Bliven K.A., Maurelli A.T. Evolution of bacterial pathogens within the human host. MicroBiol. Spectr. 2016;4:4–11. doi: 10.1128/microbiolspec.VMBF-0017-2015. PubMed DOI PMC

Emamalipour M., Seidi K., Zununi Vahed S., Jahanban-Esfahlan A., Jaymand M., Majdi H., Amoozgar Z., Chitkushev L.T., Javaheri T., Jahanban-Esfahlan R., et al. Horizontal gene transfer: From evolutionary flexibility to disease progression. Front. Cell Dev. Biol. 2020;8:229. doi: 10.3389/fcell.2020.00229. PubMed DOI PMC

Husnik F. Host-symbiont-pathogen interactions in blood-feeding parasites: Nutrition, immune cross-talk and gene exchange. Parasitology. 2018;145:1294–1303. doi: 10.1017/S0031182018000574. PubMed DOI

Schönknecht G., Weber A.P., Lercher M.J. Horizontal gene acquisitions by eukaryotes as drivers of adaptive evolution. Bioessays. 2014;36:9–20. doi: 10.1002/bies.201300095. PubMed DOI

Gilbert C., Cordaux R. Viruses as vectors of horizontal transfer of genetic material in eukaryotes. Curr. Opin. Virol. 2017;25:16–22. doi: 10.1016/j.coviro.2017.06.005. PubMed DOI

Daubin V., Szollosi G.J. Horizontal gene transfer and the history of life. Cold Spring Harb. Perspect Biol. 2016;8:a018036. doi: 10.1101/cshperspect.a018036. PubMed DOI PMC

Schott E.J., Di Lella S., Bachvaroff T.R., Amzel L.M., Vasta G.R. Lacking catalase, a protistan parasite draws on its photosynthetic ancestry to complete an antioxidant repertoire with ascorbate peroxidase. BMC Evol. Biol. 2019;19:146. doi: 10.1186/s12862-019-1465-5. PubMed DOI PMC

Butenko A., Hammond M., Field M.C., Ginger M.L., Yurchenko V., Lukeš J. Reductionist pathways for parasitism in euglenozoans? Expanded datasets provide new insights. Trends Parasitol. 2021;37:100–116. PubMed

Lukeš J., Butenko A., Hashimi H., Maslov D.A., Votýpka J., Yurchenko V. Trypanosomatids are much more than just trypanosomes: Clues from the expanded family tree. Trends Parasitol. 2018;34:466–480. doi: 10.1016/j.pt.2018.03.002. PubMed DOI

Maslov D.A., Opperdoes F.R., Kostygov A.Y., Hashimi H., Lukeš J., Yurchenko V. Recent advances in trypanosomatid research: Genome organization, expression, metabolism, taxonomy and evolution. Parasitology. 2019;146:1–27. doi: 10.1017/S0031182018000951. PubMed DOI

Kostygov A.Y., Karnkowska A., Votýpka J., Tashyreva D., Maciszewski K., Yurchenko V., Lukeš J. Euglenozoa: Taxonomy, diversity and ecology, symbioses and viruses. Open Biol. 2021;11:200407. doi: 10.1098/rsob.200407. PubMed DOI PMC

Bianchi C., Kostygov A.Y., Kraeva N., Záhonová K., Horáková E., Sobotka R., Lukeš J., Yurchenko V. An enigmatic catalase of Blastocrithidia. Mol. BioChem. Parasitol. 2019;232:111199. PubMed

Opperdoes F.R., Butenko A., Zakharova A., Gerasimov E.S., Zimmer S.L., Lukeš J., Yurchenko V. The remarkable metabolism of Vickermania ingenoplastis: Genomic predictions. Pathogens. 2021;10:68. doi: 10.3390/pathogens10010068. PubMed DOI PMC

Albanaz A.T.S., Gerasimov E.S., Shaw J.J., Sádlová J., Lukeš J., Volf P., Opperdoes F.R., Kostygov A.Y., Butenko A., Yurchenko V. Genome analysis of Endotrypanum and Porcisia spp., closest phylogenetic relatives of Leishmania, highlights the role of amastins in shaping pathogenicity. Genes. 2021;12:444. PubMed PMC

Freire A.C.G., Alves C.L., Goes G.R., Resende B.C., Moretti N.S., Nunes V.S., Aguiar P.H.N., Tahara E.B., Franco G.R., Macedo A.M., et al. Catalase expression impairs oxidative stress-mediated signalling in Trypanosoma cruzi. Parasitology. 2017;144:1498–1510. doi: 10.1017/S0031182017001044. PubMed DOI

Sádlová J., Podešvová L., Bečvář T., Bianchi C., Gerasimov E.S., Saura A., Glanzová K., Leštinová T., Matveeva N.S., Chmelová L., et al. Catalase impairs Leishmania mexicana development and virulence. Virulence. 2021;12:852–867. PubMed PMC

Horáková E., Faktorová D., Kraeva N., Kaur B., Van Den Abbeele J., Yurchenko V., Lukeš J. Catalase compromises the development of the insect and mammalian stages of Trypanosoma brucei. FEBS J. 2020;287:964–977. PubMed

Votýpka J., Klepetková H., Yurchenko V.Y., Horák A., Lukeš J., Maslov D.A. Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Protist. 2012;163:616–631. PubMed

Kostygov A., Frolov A.O., Malysheva M.N., Ganyukova A.I., Chistyakova L.V., Tashyreva D., Tesařová M., Spodareva V.V., Režnarová J., Macedo D.H., et al. Vickermania gen. nov., trypanosomatids that use two joined flagella to resist midgut peristaltic flow within the fly host. BMC Biol. 2020;18:187. PubMed PMC

Lukeš J., Tesařová M., Yurchenko V., Votýpka J. Characterization of a new cosmopolitan genus of trypanosomatid parasites, Obscuromonas gen. nov. (Blastocrithidiinae subfam. nov.) Eur. J. Protistol. 2021;79:125778. doi: 10.1016/j.ejop.2021.125778. PubMed DOI

Yurchenko V., Lukeš J., Jirků M., Maslov D.A. Selective recovery of the cultivation-prone components from mixed trypanosomatid infections: A case of several novel species isolated from Neotropical Heteroptera. Int. J. Syst. Evol. MicroBiol. 2009;59:893–909. doi: 10.1099/ijs.0.001149-0. PubMed DOI

Sayers E.W., Agarwala R., Bolton E.E., Brister J.R., Canese K., Clark K., Connor R., Fiorini N., Funk K., Hefferon T., et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 2019;47:D23–D28. doi: 10.1093/nar/gky1069. PubMed DOI PMC

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Matson F.A. Seqmagick. 2021. [(accessed on 1 November 2021)]. Available online: https://fhcrc.github.io/seqmagick/

Price M.N., Dehal P.S., Arkin A.P. FastTree 2—Approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010;5:e9490. doi: 10.1371/journal.pone.0009490. PubMed DOI PMC

Nguyen L.T., Schmidt H.A., von Haeseler A., Minh B.Q. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 2015;32:268–274. doi: 10.1093/molbev/msu300. PubMed DOI PMC

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu L., Suchard M.A., Huelsenbeck J.P. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 2012;61:539–542. PubMed PMC

Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC

Yurchenko V., Butenko A., Kostygov A.Y. Genomics of Trypanosomatidae: Where we stand and what needs to be done? Pathogens. 2021;10:1124. doi: 10.3390/pathogens10091124. PubMed DOI PMC

Marchler-Bauer A., Derbyshire M.K., Gonzales N.R., Lu S., Chitsaz F., Geer L.Y., Geer R.C., He J., Gwadz M., Hurwitz D.I., et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–D226. doi: 10.1093/nar/gku1221. PubMed DOI PMC

Lu S., Wang J., Chitsaz F., Derbyshire M.K., Geer R.C., Gonzales N.R., Gwadz M., Hurwitz D.I., Marchler G.H., Song J.S., et al. CDD/SPARCLE: The conserved domain database in 2020. Nucleic Acids Res. 2020;48:D265–D268. doi: 10.1093/nar/gkz991. PubMed DOI PMC

Eddy S.R. Accelerated profile HMM searches. PLoS Comput. Biol. 2011;7:e1002195. doi: 10.1371/journal.pcbi.1002195. PubMed DOI PMC

Sievers F., Wilm A., Dineen D., Gibson T.J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M., Soding J., et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 2011;7:539. doi: 10.1038/msb.2011.75. PubMed DOI PMC

Valverde S. DisplayR: Easy and Quick Data Exploration. 2021. [(accessed on 1 November 2021)]. Available online: http://www.displayr.com.

Valverde S., Záhonová K., Kostygov A., Ševčíková T., Yurchenko V., Eliáš M. An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr. Biol. 2016;26:2364–2369. PubMed

Woodbury W., Spencer A.K., Stahman M.A. An improved procedure using ferricyanide for detecting catalase isozymes. Anal. BioChem. 1971;44:301–305. doi: 10.1016/0003-2697(71)90375-7. PubMed DOI

Noble R.W., Gibson Q.H. The reaction of ferrous horseradish peroxidase with hydrogen peroxide. J. Biol. Chem. 1970;245:2409–2413. doi: 10.1016/S0021-9258(18)63167-9. PubMed DOI

Leatherbarrow R.J. Using linear and non-linear regression to fit biochemical data. Trends BioChem. Sci. 1990;15:455–458. doi: 10.1016/0968-0004(90)90295-M. PubMed DOI

Switala J., Loewen P.C. Diversity of properties among catalases. Arch. BioChem. Biophys. 2002;401:145–154. doi: 10.1016/S0003-9861(02)00049-8. PubMed DOI

Jumper J., Evans R., Pritzel A., Green T., Figurnov M., Ronneberger O., Tunyasuvunakool K., Bates R., Zidek A., Potapenko A., et al. Highly accurate protein structure prediction with AlphaFold. Nature. 2021;596:583–589. doi: 10.1038/s41586-021-03819-2. PubMed DOI PMC

Mirdita M., Ovchinnikov S., Steinegger M. ColabFold—Making protein folding accessible to all. BioRxiv. 2021 doi: 10.1101/2021.08.15.456425. PubMed DOI PMC

Wheeler R.J. A resource for improved predictions of Trypanosoma and Leishmania protein three-dimensional structure. PLoS ONE. 2021;16:e0259871. doi: 10.1371/journal.pone.0259871. PubMed DOI PMC

DeLano W.L. The PyMOL Molecular Graphics System. 2021. [(accessed on 1 November 2021)]. Available online: http://pymol.sourceforge.net/

Mishra S., Imlay J. Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch. BioChem. Biophys. 2012;525:145–160. doi: 10.1016/j.abb.2012.04.014. PubMed DOI PMC

Putnam C.D., Arvai A.S., Bourne Y., Tainer J.A. Active and inhibited human catalase structures: Ligand and NADPH binding and catalytic mechanism. J. Mol. Biol. 2000;296:295–309. doi: 10.1006/jmbi.1999.3458. PubMed DOI

Ivens A.C., Peacock C.S., Worthey E.A., Murphy L., Aggarwal G., Berriman M., Sisk E., Rajandream M.A., Adlem E., Aert R., et al. The genome of the kinetoplastid parasite, Leishmania major. Science. 2005;309:436–442. doi: 10.1126/science.1112680. PubMed DOI PMC

Beverley S.M. Gene amplification in Leishmania. Annu. Rev. MicroBiol. 1991;45:417–444. doi: 10.1146/annurev.mi.45.100191.002221. PubMed DOI

Vera A., Gonzalez-Montalban N., Aris A., Villaverde A. The conformational quality of insoluble recombinant proteins is enhanced at low growth temperatures. Biotechnol. Bioeng. 2007;96:1101–1106. doi: 10.1002/bit.21218. PubMed DOI

Al-Mustafa J., Sykora M., Kincaid J.R. Resonance Raman investigation of cyanide ligated beef liver and Aspergillus niger catalases. J. Biol. Chem. 1995;270:10449–10460. doi: 10.1074/jbc.270.18.10449. PubMed DOI

Jha V., Chelikani P., Carpena X., Fita I., Loewen P.C. Influence of main channel structure on H2O2 access to the heme cavity of catalase KatE of Escherichia coli. Arch. BioChem. Biophys. 2012;526:54–59. doi: 10.1016/j.abb.2012.06.010. PubMed DOI

Fita I., Rossmann M.G. The active center of catalase. J. Mol. Biol. 1985;185:21–37. doi: 10.1016/0022-2836(85)90180-9. PubMed DOI

Kalko S.G., Gelpi J.L., Fita I., Orozco M. Theoretical study of the mechanisms of substrate recognition by catalase. J. Am. Chem. Soc. 2001;123:9665–9672. doi: 10.1021/ja010512t. PubMed DOI

Chelikani P., Fita I., Loewen P.C. Diversity of structures and properties among catalases. Cell Mol. Life Sci. 2004;61:192–208. doi: 10.1007/s00018-003-3206-5. PubMed DOI PMC

Chelikani P., Donald L.J., Duckworth H.W., Loewen P.C. Hydroperoxidase II of Escherichia coli exhibits enhanced resistance to proteolytic cleavage compared to other catalases. Biochemistry. 2003;42:5729–5735. doi: 10.1021/bi034208j. PubMed DOI

Chelikani P., Carpena X., Fita I., Loewen P.C. An electrical potential in the access channel of catalases enhances catalysis. J. Biol. Chem. 2003;278:31290–31296. doi: 10.1074/jbc.M304076200. PubMed DOI

Frolov A.O., Kostygov A.Y., Yurchenko V. Development of monoxenous trypanosomatids and phytomonads in insects. Trends Parasitol. 2021;37:538–551. doi: 10.1016/j.pt.2021.02.004. PubMed DOI

Iancu L., Angelescu I.R., Paun V.I., Henríquez-Castillo C., Lavin P., Purcarea C. Microbiome pattern of Lucilia sericata (Meigen) (Diptera: Calliphoridae) and feeding substrate in the presence of the foodborne pathogen Salmonella enterica. Sci. Rep. 2021;11:15296. doi: 10.1038/s41598-021-94761-w. PubMed DOI PMC

Bai S., Yao Z., Raza M.F., Cai Z., Zhang H. Regulatory mechanisms of microbial homeostasis in insect gut. Insect Sci. 2021;28:286–301. doi: 10.1111/1744-7917.12868. PubMed DOI

Fredensborg B.L., Fossdal I.K.I., Johannesen T.B., Stensvold C.R., Nielsen H.V., Kapel C.M.O. Parasites modulate the gut-microbiome in insects: A proof-of-concept study. PLoS ONE. 2020;15:e0227561. doi: 10.1371/journal.pone.0227561. PubMed DOI PMC

Opperdoes F.R., Butenko A., Flegontov P., Yurchenko V., Lukeš J. Comparative metabolism of free-living Bodo saltans and parasitic trypanosomatids. J. Eukaryot. MicroBiol. 2016;63:657–678. doi: 10.1111/jeu.12315. PubMed DOI

Prakash K., Prajapati S., Ahmad A., Jain S.K., Bhakuni V. Unique oligomeric intermediates of bovine liver catalase. Protein. Sci. 2002;11:46–57. doi: 10.1110/ps.ps.20102. PubMed DOI PMC

Rafikov R., Kumar S., Aggarwal S., Hou Y., Kangath A., Pardo D., Fineman J.R., Black S.M. Endothelin-1 stimulates catalase activity through the PKCdelta-mediated phosphorylation of serine 167. Free Radic. Biol. Med. 2014;67:255–264. doi: 10.1016/j.freeradbiomed.2013.10.814. PubMed DOI PMC

Johnston M.A., Delwiche E.A. Isolation and characterization of the cyanide-resistant and azide-resistant catalase of Lactobacillus plantarum. J. Bacteriol. 1965;90:352–356. doi: 10.1128/jb.90.2.352-356.1965. PubMed DOI PMC

Loewen P.C., Switala J. Purification and characterization of spore-specific catalase-2 from Bacillus subtilis. BioChem. Cell Biol. 1988;66:707–714. doi: 10.1139/o88-081. PubMed DOI

Thompson V.S., Schaller K.D., Apel W.A. Purification and characterization of a novel thermo-alkali-stable catalase from Thermus brockianus. Biotechnol. Prog. 2003;19:1292–1299. doi: 10.1021/bp034040t. PubMed DOI

Ray M., Mishra P., Das P., Sabat S.C. Expression and purification of soluble bio-active rice plant catalase-A from recombinant Escherichia coli. J. Biotechnol. 2012;157:12–19. doi: 10.1016/j.jbiotec.2011.09.022. PubMed DOI

Vatsyayan P., Goswami P. Acidic pH conditions induce dissociation of the haem from the protein and destabilise the catalase isolated from Aspergillus terreus. Biotechnol. Lett. 2011;33:347–351. doi: 10.1007/s10529-010-0442-2. PubMed DOI

Lineweaver H., Burk D. The determination of enzyme dissociation constants. J. Am. Chem. Soc. 1934;56:658–666. doi: 10.1021/ja01318a036. DOI

In silico prediction of the metabolism of Blastocrithidia nonstop, a trypanosomatid with non-canonical genetic code