The genome of the ant Tetramorium bicarinatum reveals a tandem organization of venom peptides genes allowing the prediction of their regulatory and evolutionary profiles.
Ants
Chromosome-level genome
Evolution
Expression control
Peptides
Tetramorium bicarinatum
Toxins
Venom
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
20 Jan 2024
20 Jan 2024
Historique:
received:
28
08
2023
accepted:
13
01
2024
medline:
21
1
2024
pubmed:
21
1
2024
entrez:
20
1
2024
Statut:
epublish
Résumé
Venoms have evolved independently over a hundred times in the animal kingdom to deter predators and/or subdue prey. Venoms are cocktails of various secreted toxins, whose origin and diversification provide an appealing system for evolutionary researchers. Previous studies of the ant venom of Tetramorium bicarinatum revealed several Myrmicitoxin (MYRTX) peptides that gathered into seven precursor families suggesting different evolutionary origins. Analysis of the T. bicarinatum genome enabling further genomic approaches was necessary to understand the processes underlying the evolution of these myrmicitoxins. Here, we sequenced the genome of Tetramorium bicarinatum and reported the organisation of 44 venom peptide genes (vpg). Of the eleven chromosomes that make up the genome of T. bicarinatum, four carry the vpg which are organized in tandem repeats. This organisation together with the ML evolutionary analysis of vpg sequences, is consistent with evolution by local duplication of ancestral genes for each precursor family. The structure of the vpg into two or three exons is conserved after duplication events while the promoter regions are the least conserved parts of the vpg even for genes with highly identical sequences. This suggests that enhancer sequences were not involved in duplication events, but were recruited from surrounding regions. Expression level analysis revealed that most vpg are highly expressed in venom glands, although one gene or group of genes is much more highly expressed in each family. Finally, the examination of the genomic data revealed that several genes encoding transcription factors (TFs) are highly expressed in the venom glands. The search for binding sites (BS) of these TFs in the vpg promoters revealed hot spots of GATA sites in several vpg families. In this pioneering investigation on ant venom genes, we provide a high-quality assembly genome and the annotation of venom peptide genes that we think can fosters further genomic research to understand the evolutionary history of ant venom biochemistry.
Sections du résumé
BACKGROUND
BACKGROUND
Venoms have evolved independently over a hundred times in the animal kingdom to deter predators and/or subdue prey. Venoms are cocktails of various secreted toxins, whose origin and diversification provide an appealing system for evolutionary researchers. Previous studies of the ant venom of Tetramorium bicarinatum revealed several Myrmicitoxin (MYRTX) peptides that gathered into seven precursor families suggesting different evolutionary origins. Analysis of the T. bicarinatum genome enabling further genomic approaches was necessary to understand the processes underlying the evolution of these myrmicitoxins.
RESULTS
RESULTS
Here, we sequenced the genome of Tetramorium bicarinatum and reported the organisation of 44 venom peptide genes (vpg). Of the eleven chromosomes that make up the genome of T. bicarinatum, four carry the vpg which are organized in tandem repeats. This organisation together with the ML evolutionary analysis of vpg sequences, is consistent with evolution by local duplication of ancestral genes for each precursor family. The structure of the vpg into two or three exons is conserved after duplication events while the promoter regions are the least conserved parts of the vpg even for genes with highly identical sequences. This suggests that enhancer sequences were not involved in duplication events, but were recruited from surrounding regions. Expression level analysis revealed that most vpg are highly expressed in venom glands, although one gene or group of genes is much more highly expressed in each family. Finally, the examination of the genomic data revealed that several genes encoding transcription factors (TFs) are highly expressed in the venom glands. The search for binding sites (BS) of these TFs in the vpg promoters revealed hot spots of GATA sites in several vpg families.
CONCLUSION
CONCLUSIONS
In this pioneering investigation on ant venom genes, we provide a high-quality assembly genome and the annotation of venom peptide genes that we think can fosters further genomic research to understand the evolutionary history of ant venom biochemistry.
Identifiants
pubmed: 38245722
doi: 10.1186/s12864-024-10012-y
pii: 10.1186/s12864-024-10012-y
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
84Informations de copyright
© 2024. The Author(s).
Références
Schendel V, Rash LD, Jenner RA, Undheim EAB. The diversity of venom: The importance of behavior and venom system morphology in understanding its ecology and evolution. Toxins. 2019;11(11):666.
pubmed: 31739590
pmcid: 6891279
doi: 10.3390/toxins11110666
Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG. Complex cocktails: The evolutionary novelty of venoms. Trends Ecol Evol. 2013;28:219–29.
pubmed: 23219381
doi: 10.1016/j.tree.2012.10.020
Tasoulis T, Pukala TL, Isbister GK. Investigating Toxin Diversity and Abundance in Snake Venom Proteomes. Front Pharmacol. 2022;12:768015.
pubmed: 35095489
pmcid: 8795951
doi: 10.3389/fphar.2021.768015
Walker AA. The evolutionary dynamics of venom toxins made by insects and other animals. Biochem Soc Trans. 2020;48:1353–65.
pubmed: 32756910
doi: 10.1042/BST20190820
Walker AA, Madio B, Jin J, Undheim EAB, Fry BG, King GF. Melt with this kiss: Paralyzing and liquefying venom of the Assassin bug Pristhesancus plagipennis (Hemiptera: Reduviidae). Mol Cell Proteomics. 2017;16:552–66.
pubmed: 28130397
pmcid: 5383778
doi: 10.1074/mcp.M116.063321
Walker AA, Robinson SD, Paluzzi JPV, Merritt DJ, Nixon SA, Schroeder CI, et al. Production, composition, and mode of action of the painful defensive venom produced by a limacodid caterpillar, Doratifera vulnerans. Proc Natl Acad Sci USA. 2021;118:1–12.
doi: 10.1073/pnas.2023815118
Walker AA, Dobson J, Jin J, Robinson SD, Herzig V, Vetter I, et al. Buzz kill: Function and proteomic composition of venom from the giant assassin fly Dolopus genitalis (Diptera: Asilidae). Toxins. 2018;10:1–17.
doi: 10.3390/toxins10110456
Drukewitz SH, Bokelmann L, Undheim EAB, Von Reumont BM. Toxins from scratch? Diverse, multimodal gene origins in the predatory robber fly Dasypogon diadema indicate a dynamic venom evolution in dipteran insects. GigaScience. 2019;8:1–13.
doi: 10.1093/gigascience/giz081
Martinson EO, Mrinalini, Kelkar YD, Chang CH, Werren JH. The evolution of venom by co-option of single-copy genes. Curr Biol. 2017;27:2007-2013.e8.
pubmed: 28648823
pmcid: 5719492
doi: 10.1016/j.cub.2017.05.032
Koludarov I, Velasque M, Senoner T, Timm T, Greve C, Hamadou AB, et al. Prevalent bee venom genes evolved before the aculeate stinger and eusociality. BMC Biol. 2023;21(1):229.
pubmed: 37867198
pmcid: 10591384
doi: 10.1186/s12915-023-01656-5
Touchard A, Aili SR, Fox EGP, Escoubas P, Orivel J, Nicholson GM, et al. The biochemical toxin arsenal from ant venoms. Toxins. 2016;8:1–28.
doi: 10.3390/toxins8010030
GODFRAY HCJ. The Immature Parasitoid. In: Parasitoids. Princeton University Press; 1994. p. 225–59.
Robinson SD, Mueller A, Clayton D, Starobova H, Hamilton BR, Payne RJ, et al. A comprehensive portrait of the venom of the giant red bull ant, Myrmecia gulosa, reveals a hyperdiverse hymenopteran toxin gene family. Sci Adv. 2018;4:1–12.
doi: 10.1126/sciadv.aau4640
von Reumont BM, Dutertre S, Koludarov I. Venom profile of the European carpenter bee Xylocopa violacea: Evolutionary and applied considerations on its toxin components. Toxicon: X. 2022;14:100117.
Perez-Riverol A, dos Santos-Pinto JRA, Lasa AM, Palma MS, Brochetto-Braga MR. Wasp venomic: Unravelling the toxins arsenal of Polybia paulista venom and its potential pharmaceutical applications. J Proteomics. 2017;161:88–103.
pubmed: 28435107
doi: 10.1016/j.jprot.2017.04.016
Jensen T, Walker AA, Nguyen SH, Jin AH, Deuis JR, Vetter I, et al. Venom chemistry underlying the painful stings of velvet ants (Hymenoptera: Mutillidae). Cell Mol Life Sci. 2021;78:5163–77.
pubmed: 33970306
doi: 10.1007/s00018-021-03847-1
Guido-Patiño JC, Plisson F. Profiling hymenopteran venom toxins: Protein families, structural landscape, biological activities, and pharmacological benefits. Toxicon: X. 2022;14:100119.
Touchard A, Téné N, Song PCT, Lefranc B, Leprince J, Treilhou M, et al. Deciphering the molecular diversity of an ant venom peptidome through a venomics approach. J Proteome Res. 2018;17:3503–16.
pubmed: 30149710
doi: 10.1021/acs.jproteome.8b00452
Barassé V, Touchard A, Téné N, C K, Paquet F, Tysklind N, et al. Venomics survey of six myrmicine ants provides insights into the molecular and structural diversity of their peptide toxins. Insect Biochem Mol Biol. 2022; 151:103876
Touchard A, Aili SR, Téné N, Barassé V, Klopp C, Dejean A, et al. Venom peptide repertoire of the European myrmicine ant Manica rubida: Identification of insecticidal toxins. J Proteome Res. 2020;19:1800–11.
pubmed: 32182430
doi: 10.1021/acs.jproteome.0c00048
Bonnafé E, Téné N, Berger F, Rifflet A, Guilhaudis L, Ségalas-Milazzo I, et al. Biochemical and biophysical combined study of bicarinalin, an ant venom antimicrobial peptide. Peptides. 2016;79:103–13.
pubmed: 27058430
doi: 10.1016/j.peptides.2016.04.001
Duraisamy K, Singh K, Kumar M, Lefranc B, Bonnafé E, Treilhou M, et al. P17 induces chemotaxis and differentiation of monocytes via MRGPRX2-mediated mast cell–line activation. J Allergy Clin Immunol. 2022;149:275–91.
pubmed: 34111449
doi: 10.1016/j.jaci.2021.04.040
Hadzić T, Park D, Abruzzi KC, Yang L, Trigg JS, Rohs R, et al. Genome-wide features of neuroendocrine regulation in Drosophila by the basic helix-loop-helix transcription factor DIMMED. Nucleic Acids Res. 2015;43:2199–215.
pubmed: 25634895
pmcid: 4344488
doi: 10.1093/nar/gku1377
Johnson DM, Wells MB, Fox R, Lee JS, Loganathan R, Levings D, et al. CrebA increases secretory capacity through direct transcriptional regulation of the secretory machinery, a subset of secretory cargo, and other key regulators. Traffic. 2020;21:560–77.
pubmed: 32613751
pmcid: 8142552
doi: 10.1111/tra.12753
Petersen UM, Kadalayil L, Rehorn KP, Hoshizaki DK, Reuter R, Engström Y. Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif. EMBO J. 1999;18:4013–22.
pubmed: 10406806
pmcid: 1171477
doi: 10.1093/emboj/18.14.4013
Senger K, Harris K, Levine M. GATA factors participate in tissue-specific immune responses in Drosophila larvae. Proc Natl Acad Sci USA. 2006;103:15957–62.
pubmed: 17032752
pmcid: 1635109
doi: 10.1073/pnas.0607608103
Rus F, Flatt T, Tong M, Aggarwal K, Okuda K, Kleino A, et al. Ecdysone triggered PGRP-LC expression controls Drosophila innate immunity. EMBO J. 2013;32:1626–38.
pubmed: 23652443
pmcid: 3671248
doi: 10.1038/emboj.2013.100
Senger K, Armstrong GW, Rowell WJ, Kwan JM, Markstein M, Levine M. Immunity regulatory DNAs share common organizational features in Drosophila. Mol Cell. 2004;13:19–32.
pubmed: 14731391
doi: 10.1016/S1097-2765(03)00500-8
Myllymäki H, Rämet M. JAK/STAT Pathway in Drosophila immunity. Scand J Immunol. 2014;79:377–85.
pubmed: 24673174
doi: 10.1111/sji.12170
Minakhina S, Tan W, Steward R. JAK/STAT and the GATA factor Pannier control hemocyte maturation and differentiation in Drosophila. Dev Biol. 2011;352:308–16.
pubmed: 21295568
pmcid: 3065540
doi: 10.1016/j.ydbio.2011.01.035
Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J. Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci. 2016;73:3221–47.
pubmed: 27100828
pmcid: 4967105
doi: 10.1007/s00018-016-2223-0
Suryamohan K, Krishnankutty SP, Guillory J, Jevit M, Schröder MS, Wu M, et al. The Indian cobra reference genome and transcriptome enables comprehensive identification of venom toxins. Nat Genet. 2020;52:106–17.
pubmed: 31907489
pmcid: 8075977
doi: 10.1038/s41588-019-0559-8
Hargreaves AD, Swain MT, Hegarty MJ, Logan DW, Mulley JF. Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biol Evol. 2014;6:2088–95.
pubmed: 25079342
pmcid: 4231632
doi: 10.1093/gbe/evu166
Ashwood LM, Elnahriry KA, Stewart ZK, Shafee T, Naseem MU, Szanto T, et al. Genomic, functional and structural analyses elucidate evolutionary innovation within the sea anemone 8 toxin family. BMC Biol. 2023;21(1):121.
pubmed: 37226201
pmcid: 10210398
doi: 10.1186/s12915-023-01617-y
Gendreau KL, Haney RA, Schwager EE, Wierschin T, Stanke M, Richards S, et al. House spider genome uncovers evolutionary shifts in the diversity and expression of black widow venom proteins associated with extreme toxicity. BMC Genomics. 2017;18(1):178.
pubmed: 28209133
pmcid: 5314461
doi: 10.1186/s12864-017-3551-7
Pardos-Blas JR, Irisarri I, Abalde S, Afonso CML, Tenorio MJ, Zardoya R. The genome of the venomous snail Lautoconus ventricosus sheds light on the origin of conotoxin diversity. GigaScience. 2021;10:1–15.
doi: 10.1093/gigascience/giab037
Robinson ASD, Deuis JR, Touchard A, Keramidas A, Mueller A, Schroeder C, et al. Ant venoms contain vertebrate-specific pain-causing sodium channel toxins. Nat Comm. 2023;14(1):2977.
doi: 10.1038/s41467-023-38839-1
Shew CJ, Carmona-Mora P, Soto DC, Mastoras M, Roberts E, Rosas J, et al. Diverse molecular mechanisms contribute to differential expression of Human duplicated genes. Mol Biol Evol. 2021;38:3060–77.
pubmed: 34009325
pmcid: 8321529
doi: 10.1093/molbev/msab131
Lan X, Pritchard JK. Coregulation of tandem duplicate genes slows evolution of subfunctionalization in mammals. Science. 2016;352:1009–13.
pubmed: 27199432
pmcid: 5182070
doi: 10.1126/science.aad8411
Kocabas A, Duarte T, Kumar S, Hynes MA. Widespread differential expression of coding region and 3’ UTR sequences in neurons and other tissues. Neuron. 2015;88:1149–56.
pubmed: 26687222
doi: 10.1016/j.neuron.2015.10.048
Ji S, Yang Z, Gozali L, Kenney T, Kocabas A, Park CJ, et al. Distinct expression of select and transcriptome-wide isolated 3’UTRs suggests critical roles in development and transition states. PLoS ONE. 2021;16(5):e0250669.
pubmed: 33951080
pmcid: 8099112
doi: 10.1371/journal.pone.0250669
Ascoët S, Touchard A, Téné N, Lefranc B, Leprince J, Paquet F, et al. The mechanism underlying toxicity of a venom peptide against insects reveals how ants are master at disrupting membranes. iScience. 2023;26(3):106157.
pubmed: 36879819
pmcid: 9985030
doi: 10.1016/j.isci.2023.106157
Lee KS, Kim BY, Yoon HJ, Choi YS, Jin BR. Secapin, a bee venom peptide, exhibits anti-fibrinolytic, anti-elastolytic, and anti-microbial activities. Dev Comp Immunol. 2016;63:27–35.
pubmed: 27208884
doi: 10.1016/j.dci.2016.05.011
Baracchi D, Francese S, Turillazzi S. Beyond the antipredatory defence: Honey bee venom function as a component of social immunity. Toxicon. 2011;58:550–7.
pubmed: 21925197
doi: 10.1016/j.toxicon.2011.08.017
Baracchi D, Mazza G, Turillazzi S. From individual to collective immunity: The role of the venom as antimicrobial agent in the Stenogastrinae wasp societies. J Insect Physiol. 2012;58:188–93.
pubmed: 22108024
doi: 10.1016/j.jinsphys.2011.11.007
Lynch M, O’Hely M, Walsh B, Force A. The probability of preservation of a newly arisen gene duplicate. Genetics. 2001;159:1789–804.
pubmed: 11779815
pmcid: 1461922
doi: 10.1093/genetics/159.4.1789
Jackson TNW, Koludarov I. How the toxin got its toxicity. Front Pharmacol. 2020;11:574925.
pubmed: 33381030
pmcid: 7767849
doi: 10.3389/fphar.2020.574925
Casewell NR, Wagstaff SC, Harrison RA, Renjifo C, Wuster W. Domain loss facilitates accelerated evolution and neofunctionalization of duplicate snake venom metalloproteinase toxin Genes. Mol BiolEvol. 2011;28:2637–49.
doi: 10.1093/molbev/msr091
Lynch VJ. Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol. 2007;7(1):1–14.
doi: 10.1186/1471-2148-7-2
Gopalan SS, Perry BW, Schield DR, Smith CF, Mackessy SP, Castoe TA. Origins, genomic structure and copy number variation of snake venom myotoxins. Toxicon. 2022;216:92–106.
pubmed: 35820472
doi: 10.1016/j.toxicon.2022.06.014
Ye X, Yang Y, Zhao C, Xiao S, Sun YH, He C, et al. Genomic signatures associated with maintenance of genome stability and venom turnover in two parasitoid wasps. Nat Commun. 2022;13(1):6417.
pubmed: 36302851
pmcid: 9613689
doi: 10.1038/s41467-022-34202-y
Peters RS, Krogmann L, Mayer C, Donath A, Gunkel S, Meusemann K, et al. Evolutionary History of the Hymenoptera. Curr Biol. 2017;27:1013–8.
pubmed: 28343967
doi: 10.1016/j.cub.2017.01.027
Loker R, Mann RS. Divergent expression of paralogous genes by modification of shared enhancer activity through a promoter-proximal silencer. Curr Biol. 2022;32(16):3545-3555.e4.
pubmed: 35853455
pmcid: 9398998
doi: 10.1016/j.cub.2022.06.069
Margres MJ, Rautsaw RM, Strickland JL, Mason AJ, Schramer TD, Hofmann EP, et al. The Tiger Rattlesnake genome reveals a complex genotype underlying a simple venom phenotype. Proc Natl Acad Sci USA. 2021;118(4):e2014634118.
pubmed: 33468678
pmcid: 7848695
doi: 10.1073/pnas.2014634118
Winnepenninckx B, Backeljau T, De Wachter R. Extraction of high molecular weight DNA from molluscs. Trends Genet. 1993;12:407.
Zimin AV, Puiu D, Luo M-C, Zhu T, Koren S, Marçais G, et al. Hybrid assembly of the large and highly repetitive genome of Aegilops tauschii, a progenitor of bread wheat, with the MaSuRCA mega-reads algorithm. Genome Res. 2017;27:787–92.
pubmed: 28130360
pmcid: 5411773
doi: 10.1101/gr.213405.116
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
Mapleson D, Garcia Accinelli G, Kettleborough G, Wright J, Clavijo BJ. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies. Bioinformatics. 2017;33:574–6.
pubmed: 27797770
doi: 10.1093/bioinformatics/btw663
Durand NC, Shamim MS, Machol I, Rao SSP, Huntley MH, Lander ES, et al. Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Syst. 2016;3:95–8.
pubmed: 27467249
pmcid: 5846465
doi: 10.1016/j.cels.2016.07.002
Dudchenko O, Batra SS, Omer AD, Nyquist SK, Hoeger M, Durand NC, et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science. 2017;356:92–5.
pubmed: 28336562
pmcid: 5635820
doi: 10.1126/science.aal3327
Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci USA. 2020;117:9451–7.
pubmed: 32300014
pmcid: 7196820
doi: 10.1073/pnas.1921046117
Tarailo‐Graovac M, Chen N. Using RepeatMasker to identify repetitive elements in genomic Sequences. CP in Bioinformatics. 2009;Mar Chapter 4:4.10.1–4.10.14.
Cantarel BL, Korf I, Robb SMC, Parra G, Ross E, Moore B, et al. MAKER: An easy-to-use annotation pipeline designed for emerging model organism genomes. Genome Res. 2008;18:188–96.
pubmed: 18025269
pmcid: 2134774
doi: 10.1101/gr.6743907
Slater G, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005;6:31.
pubmed: 15713233
pmcid: 553969
doi: 10.1186/1471-2105-6-31
Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907–15.
pubmed: 31375807
pmcid: 7605509
doi: 10.1038/s41587-019-0201-4
Dobin A, Davis CA, Schlesinger F, Drenkow J, Zaleski C, Jha S, et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013;29:15–21.
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, Van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511–5.
pubmed: 20436464
pmcid: 3146043
doi: 10.1038/nbt.1621
Hoff KJ, Lomsadze A, Borodovsky M, Stanke M. Whole-genome annotation with BRAKER. Methods Mol Biol. 2019;1962:65–95.
pubmed: 31020555
pmcid: 6635606
doi: 10.1007/978-1-4939-9173-0_5
Tamura K, Stecher G, Kumar S. MEGA11: Molecular evolutionary genetics analysis version 11. Mol Biol Evol. 2021;38:3022–7.
pubmed: 33892491
pmcid: 8233496
doi: 10.1093/molbev/msab120
Linhart C, Halperin Y, Shamir R. Transcription factor and microRNA motif discovery: The Amadeus platform and a compendium of metazoan target sets. Genome Res. 2008;18:1180–9.
pubmed: 18411406
pmcid: 2493407
doi: 10.1101/gr.076117.108