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[en] We present a reference genome assembly from an individual male Violet Carpenter Bee (Xylocopa violacea, Linnaeus 1758). The assembly is 1.02 gigabases in span. 48% of the assembly is scaffolded into 17 pseudo-chromosomal units. The mitochondrial genome has also been assembled and is 21.8 kilobases in length. The genome is highly repetitive, likely representing a highly heterochromatic architecture expected of bees from the genus Xylocopa. We also use an evidence-based methodology to annotate 10,152 high confidence coding genes. This genome was sequenced as part of the pilot project of the European Reference Genome Atlas (ERGA) and represents an important addition to the genomic resources available for Hymenoptera.
Disciplines :
Zoology
Author, co-author :
Nash, Will J ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK. will.nash@earlham.ac.uk
Man, Angela ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
McTaggart, Seanna ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Baker, Kendall ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Barker, Tom; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Catchpole, Leah; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Durrant, Alex; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Gharbi, Karim ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Irish, Naomi; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Kaithakottil, Gemy; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Ku, Debby ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Providence, Aaliyah ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Shaw, Felix; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Swarbreck, David ; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
Watkins, Chris; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK
McCartney, Ann M; Genomics Institute, University of California, Santa Cruz, CA, 95060, USA
Formenti, Giulio; The Vertebrate Genome Laboratory, The Rockefeller University, 1240 York Ave, New York, NY, 10065, USA ; Department of Biology, University of Florence, Sesto Fiorentino, Italy
Mouton, Alice ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement (Arlon Campus Environnement) > Socio-économie, Environnement et Développement (SEED) ; Department of Biology, University of Florence, Sesto Fiorentino, Italy
Vella, Noel; Conservation Biology Research Group, Biology Department, University of Malta, Msida, MSD 2080, Malta
von Reumont, Björn M; LOEWE Center for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325, Frankfurt, Germany ; Applied Bioinformatics Group, Faculty of Biological Sciences, Goethe University Frankfurt, Max-von-Laue-Str. 13, 60438, Frankfurt, Germany
Vella, Adriana; Conservation Biology Research Group, Biology Department, University of Malta, Msida, MSD 2080, Malta. adriana.vella@um.edu.mt
Haerty, Wilfried; The Earlham Institute, Norwich Research Park, Colney Lane, Norwich, NR4 7UZ, UK. wilfried.haerty@earlham.ac.uk ; School of Biological Sciences, The University of East Anglia, Norwich, NR4 7TJ, UK. wilfried.haerty@earlham.ac.uk
RCUK | Biotechnology and Biological Sciences Research Council Innovate UK Deutsche Forschungsgemeinschaft
Funding text :
We acknowledge Fiona Fraser (Earlham Institute, Norwich) and Michael Quail (Wellcome Sanger Institute, Hinxton) for valuable conversations and advice in developing Hi-C library preparation. The authors would also like to acknowledge the GRiT (Wellcome Sanger Institute, Hinxton), particularly Jo Wood, Tom Mathers, Dominic Absolon, Camilla Santos, Michael Paulini for invaluable mentorship in Hi-C scaffolding and curation. The authors also acknowledge Kamil Hepak (Norwich Bioscience Institutes, Scientific Computing) for significant HPC support.The authors acknowledge support from the Biotechnology and Biological Sciences Research Council (BBSRC), part of UK Research and Innovation, Core Capability Grant BB/CCG2220/1 at the Earlham Institute and its constituent work packages (BBS/E/T/000PR9818 and BBS/E/T/000PR9819), and the Core Capability Grant BB/CCG1720/1 and the National Capability at the Earlham Institute BBS/E/T/000PR9816 (NC1\u2014Supporting EI\u2019s ISPs and the UK Community with Genomics and Single Cell Analysis), BBS/E/T/000PR9811 (NC4\u2014Enabling and Advancing Life Scientists in data-driven research through Advanced Genomics and Computational Training), and BBS/E/T/000PR9814 (NC 3 - Development and deployment of versatile digital platforms for \u2018omics-based data sharing and analysis). Authors also acknowledge support from BBSRC Core Capability Grant BB/CCG1720/1 and the work delivered via the Scientific Computing group, as well as support for the physical HPC infrastructure and data centre delivered via the NBI Computing infrastructure for Science (CiS) group. AV and NV acknowledge funding from the BioCon_Innovate Research Excellence Grant (I18LU06-01) from the University of Malta. BMvR acknowledges funding from the DFG (RE3454/6-1).
D. Alberoni F. Gaggìa L. Baffoni M.M. Modesto B. Biavati D. Di Gioia Bifidobacterium xylocopae sp. nov. and Bifidobacterium aemilianum sp. nov., from the carpenter bee (Xylocopa violacea) digestive tract Syst Appl Microbiol 2019 42 205 216 30551956
M. Aouar-Sadli K. Louadi S.-E. Doumandji Pollination of the broad bean (Vicia faba L. var. major)(Fabaceae) by wild bees and honey bees (Hymenoptera: Apoidea) and its impact on the seed production in the Tizi-Ouzou area (Algeria) Afr J Agric Res 2008 3 266 272
A.M. Ardila-Garcia G.J. Umphrey T.R. Gregory An expansion of the genome size dataset for the insect order Hymenoptera, with a first test of parasitism and eusociality as possible constraints Insect Mol Biol 2010 19 337 346 1:CAS:528:DC%2BC3cXmsF2ru7Y%3D 20201980
A. Astashyn E.S. Tvedte D. Sweeney V. Sapojnikov N. Bouk V. Joukov et al. Rapid and sensitive detection of genome contamination at scale with FCS-GX Genome Biol 2024 25 60 1:CAS:528:DC%2BB2cXkslGltr0%3D 38409096 10898089
R.Z. Bamarni M.A. Elsaiegh A survey and phenotypic study of carpenter bee species recorded in Kzo village and its environs/Dohuk Governorate–Iraq NTU J. Agric Vet Sci 2022 2 1 4
J. Banaszak W.B. Cibicka L. Twerd Possible expansion of the range of Xylocopa violacea L. (Hymenoptera, Apiformes, Apidae) in Europe Turk Zool Derg 2019 43 650 656
Böhne A, Fernández R, Leonard JA, McCartney AM, McTaggart S, Melo-Ferreira J et al. (2024) Contextualising samples: Supporting reference genomes of European biodiversity through sample and associated metadata collection. bioRxiv: 2023.06.28.546652. https://doi.org/10.1101/2023.06.28.546652
A.M. Bolger M. Lohse B. Usadel Trimmomatic: a flexible trimmer for Illumina sequence data Bioinformatics 2014 30 2114 2120 1:CAS:528:DC%2BC2cXht1Sqt7nP 24695404 4103590
B. Bushnell BBMap: A Fast, Accurate, Splice-Aware Aligner 2014 Berkeley, CA (United States) Lawrence Berkeley National Lab. (LBNL)
G. Ceballos P.R. Ehrlich Mutilation of the tree of life via mass extinction of animal genera Proc Natl Acad Sci USA 2023 120 e2306987120 1:CAS:528:DC%2BB3sXitVKgurzP 37722053 10523489
B. Cederberg Others The carpenter bees Xylocopa valga and X. violacea-climate refugees or labour migrants in Sweden (Hymenoptera: Apidae) Entomol Tidskr 2018 139 65 72
H. Cheng G.T. Concepcion X. Feng H. Zhang H. Li Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm Nat Methods 2021 18 170 175 1:CAS:528:DC%2BB3MXis1OntL0%3D 33526886 7961889
M.S. Cunha D.C. Cardoso M.P. Cristiano L.A. de Oliveira Campos D.M. Lopes The Bee Chromosome database (Hymenoptera: Apidae) Apidologie 2021 52 493 502
S. Dar G. Mir M. Parry M.A. Sofi S.A. Padder Nest distribution and nesting habits of Xylocopa violacea (Donovan), Fabricius (Hymenoptera: Apidae) in Kashmir valley J Exp Zool India 2016 9 155 162
N.C. Durand M.S. Shamim I. Machol S.S.P. Rao M.H. Huntley E.S. Lander et al. Juicer Provides a One-Click System for Analyzing Loop-Resolution Hi-C Experiments Cell Syst 2016 3 95 98 1:CAS:528:DC%2BC2sXhtFKksbk%3D 27467249 5846465
Erkoc P, von Reumont BM, Lüddecke T, Henke M, Ulshöfer T, Vilcinskas A et al. (2022) The pharmacological potential of novel melittin variants from the honeybee and solitary bees against inflammation and cancer. Toxins 14
G. Formenti K. Theissinger C. Fernandes I. Bista A. Bombarely C. Bleidorn et al. The era of reference genomes in conservation genomics Trends Ecol Evol 2022 37 197 202 1:CAS:528:DC%2BB38XisFyku7%2FF 35086739
D. Gerling H.H.W. Velthuis A. Hefetz Bionomics of the large carpenter bees of the genus xylocopa Annu Rev Entomol 1989 34 163 190
V.E. Gokhman Chromosome study of the hymenoptera: history, current state, perspectives Biol Bull Rev 2023 13 247 257
L. Granata Le divisioni degli spermatociti di ‘Xylocopa violacea’ L Biologica Torino 1909 2 1 12
C.A. Hallmann M. Sorg E. Jongejans H. Siepel N. Hofland H. Schwan et al. More than 75 percent decline over 27 years in total flying insect biomass in protected areas PLoS One 2017 12 29045418 5646769
C.A. Halsch A.M. Shapiro J.A. Fordyce C.C. Nice J.H. Thorne D.P. Waetjen et al. Insects and recent climate change Proc Natl Acad Sci USA 2021 118 e2002543117 1:CAS:528:DC%2BB3MXhsVCisLc%3D 33431560 7812774
M.Y. Handy D.L. Sbardellati M. Yu N.W. Saleh M.M. Ostwald R.L. Vannette Incipiently social carpenter bees (Xylocopa) host distinctive gut bacterial communities and display geographical structure as revealed by full-length PacBio 16S rRNA sequencing Mol Ecol 2023 32 1530 1543 1:CAS:528:DC%2BB38XivVWnt77L 36239475
J.-A.C. Holley M.N. Jackson A.T. Pham S.C. Hatcher N.A. Moran Carpenter Bees (Xylocopa) Harbor a Distinctive Gut Microbiome Related to That of Honey Bees and Bumble Bees Appl Environ Microbiol 2022 88 e0020322 35758673
H. Hoshiba H. Imai Chromosome evolution of bees and wasps (Hymenoptera, apocrita) on the basis of C-banding pattern analyses Jpn J Entomol 1993 61 465 492
S.D. Jackman B.P. Vandervalk H. Mohamadi J. Chu S. Yeo S.A. Hammond et al. ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter Genome Res 2017 27 768 777 1:CAS:528:DC%2BC2sXhtFyjsrrO 28232478 5411771
J.T. Kerr A. Pindar P. Galpern L. Packer S.G. Potts S.M. Roberts et al. Climate change impacts on bumblebees converge across continents Science 2015 349 177 180 1:CAS:528:DC%2BC2MXhtFWqtr%2FP 26160945
W.E. Kerr Z.V. da Silveira Karyotypic evolution of bees and corresponding taxonomic implications Evolution 1972 26 197 202 28555733
Kleprlíková L, Vrabec V (2020) Bee spread continues-new records of Xylocopinae (Hymenoptera: Apidae) in the Czech Republic. In: Conference paper, 11th Workshop on Biodiversity, Jevany, researchgate.net, p
I. Koludarov M. Velasque T. Senoner T. Timm C. Greve A.B. Hamadou et al. Prevalent bee venom genes evolved before the aculeate stinger and eusociality BMC Biol 2023 21 37867198 10591384
C.G. Kumbkarni Cytological Studies in Hymenoptera: Part II: Cytology of parthenogenesis in the carpenter-bee, Xylocopa fenesterata (Fabre) Cytologica 1965 30 222 228
Latreille PA (1802). Histoire naturelle, générale et particulière des crustacés et des insectes. de l’imprimerie de F. Dufart.
P. Lehmann T. Ammunét M. Barton A. Battisti S.D. Eigenbrode J.U. Jepsen et al. Complex responses of global insect pests to climate warming Front Ecol Environ 2020 18 141 150
R. Leys S.J. Cooper M.P. Schwarz Molecular phylogeny of the large carpenter bees, genus Xylocopa (Hymenoptera: apidae), based on mitochondrial DNA sequences Mol Phylogenet Evol 2000 17 407 418 1:CAS:528:DC%2BD3cXptVygu74%3D 11133195
R. Leys S.J.B. Cooper M.P. Schwarz Molecular phylogeny and historical biogeography of the large carpenter bees, genus Xylocopa (Hymenoptera: Apidae) Biol J Linn Soc Lond 2002 77 249 266
Linnaeus C (1758). Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis, 10th edn. Laurentii Salvii: Holmiae.
V.A. Lukhtanov E.A. Pazhenkova Diversity and evolution of telomeric motifs and telomere DNA organization in insects Biol J Linn Soc Lond 2023 140 536 555
Lukhtanov VA (2022) Diversity and evolution of telomere and subtelomere DNA sequences in insects. bioRxiv: 2022.04.08.487650. https://doi.org/10.1101/2022.04.08.487650
Malabusini S, Palamara Mesiano M, Zanovello D, Giuliani C, Fico G, Giovanetti M et al. (2019) Flower selection of Xylocopa violacea: aromatic and ornamental plants as resources in a botanic garden. In: Landscape management for functional biodiversity, IOBC-WPRS, pp 41–45
M. Manni M.R. Berkeley M. Seppey F.A. Simão E.M. Zdobnov BUSCO Update: Novel and Streamlined Workflows along with Broader and Deeper Phylogenetic Coverage for Scoring of Eukaryotic, Prokaryotic, and Viral Genomes Mol Biol Evol 2021 38 4647 4654 1:CAS:528:DC%2BB38XhslaktbzF 34320186 8476166
M. Martin Cutadapt removes adapter sequences from high-throughput sequencing reads EMBnet J 2011 17 10 12
Mc Cartney AM, Formenti G, Mouton A, Ciofi C, Waterhouse RM, Mazzoni CJ et al. (2024) The European Reference Genome Atlas: piloting a decentralised approach to equitable biodiversity genomics. bioRxiv: 2023.09.25.559365v4. https://doi.org/10.1101/2023.09.25.559365
F.A.B. von Meijenfeldt K. Arkhipova D.D. Cambuy F.H. Coutinho B.E. Dutilh Robust taxonomic classification of uncharted microbial sequences and bins with CAT and BAT Genome Biol 2019 20
Michener CD (2007) The Bees of the World. Johns Hopkins University Press
V.E. Mullin W. Stephen A.N. Arce W. Nash C. Raine D.G. Notton et al. First large‐scale quantification study of DNA preservation in insects from natural history collections using genome‐wide sequencing Methods Ecol Evol 2022 14 360 371
Ollerton J (2021) Pollinators and Pollination: Nature and Society. Pelagic Publishing Ltd
C.L. Outhwaite P. McCann T. Newbold Agriculture and climate change are reshaping insect biodiversity worldwide Nature 2022 605 97 102 1:CAS:528:DC%2BB38XhtVGnsLfE 35444282
J.A. Pereira N.M. Travenzoli M.P. de Oliveira H. de Azevedo Werneck T.M.F. Salomão D.M. Lopes Molecular cytogenetics in the study of repetitive sequences helping to understand the evolution of heterochromatin in Melipona (Hymenoptera, Meliponini) Genetica 2021 149 55 62 1:CAS:528:DC%2BB3MXmt1ahtbY%3D 33449238
M.C.A. Piccoli V.B. Bardella D.C. Cabral-de-Mello Repetitive DNAs in Melipona scutellaris (Hymenoptera: Apidae: Meliponidae): chromosomal distribution and test of multiple heterochromatin amplification in the genus Apidologie 2018 49 497 504 1:CAS:528:DC%2BC1cXovVWlsrw%3D
G.D. Powney C. Carvell M. Edwards R.K.A. Morris H.E. Roy B.A. Woodcock et al. Widespread losses of pollinating insects in Britain Nat Commun 2019 10 30914632 6435717
Praz C, Müller A, Hermann M, Neumeyer-Funk R, Bénon D, Amiet F et al. (2022) Swiss National Apoidea Databank. Version 1.5
B.M. von Reumont S. Dutertre I. Koludarov Venom profile of the European carpenter bee Xylocopa violacea: Evolutionary and applied considerations on its toxin components Toxicon X 2022 14 100117
A. Rhie B.P. Walenz S. Koren A.M. Phillippy Merqury: reference-free quality, completeness, and phasing assessment for genome assemblies Genome Biol 2020 21 1:CAS:528:DC%2BB3cXhvVKmu7rF 32928274 7488777
O. Rollin S. Vray N. Dendoncker D. Michez M. Dufrêne P. Rasmont Drastic shifts in the Belgian bumblebee community over the last century Biodivers Conserv 2020 29 2553 2573
F. Shaw A. Etuk A. Minotto A. Gonzalez-Beltran D. Johnson P. Rocca-Serra et al. COPO: a metadata platform for brokering FAIR data in the life sciences F1000Res 2020 9 495
S. Skendžić M. Zovko I.P. Živković V. Lešić D. Lemić The impact of climate change on agricultural insect pests Insects 2021 12 440 34066138 8150874
T. Sless S. Rehan Phylogeny of the carpenter bees (Apidae: Xylocopinae) highlights repeated evolution of sociality Biol Lett 2023 19 20230252 1:CAS:528:DC%2BB3sXitFKis7fN 37643643 10465191
M.G. Tavares C.R. Carvalho Soares FAF Genome size variation in Melipona species (Hymenoptera: Apidae) and sub-grouping by their DNA content Apidologie 2010 41 636 642 1:CAS:528:DC%2BC3MXnslGnsg%3D%3D
S. Tezcan I. Skyrpan New Locality Records For Xylocopa (Hymenoptera: Apidae: Xylocopinae) Fauna of Turkey. Біологічні студії / Stud Biologica 2022 16 3 12
Travenzoli N.M. Cunha M.S. Teixeira L.V. Brito R.M. Oldroyd B. Campos LAO et al. Cytogenetic characterization of Austroplebeia australis: evolutionary hints from a stingless bee outside the Neotropical region Apidologie (Celle) 2022 53 1 8
Uliano-Silva M. Ferreira JGRN Krasheninnikova K. Darwin Tree of Life Consortium G. Formenti L. Abueg et al. MitoHiFi: a python pipeline for mitochondrial genome assembly from PacBio high fidelity reads BMC Bioinforma 2023 24 1:CAS:528:DC%2BB3sXhsFCltbnM
P. Vargas I. Liberal C. Ornosa J.M. Gómez Flower specialisation: the occluded corolla of snapdragons (Antirrhinum) exhibits two pollinator niches of large long-tongued bees Plant Biol 2017 19 787 797 1:CAS:528:DC%2BC2sXht1yktbzI 28590517
S. Vicidomini Biology of Xylocopa violacea (Hymenoptera): In‐nest ethology Ital J Zool 1996 63 237 242
M.R. Vollger P. Kerpedjiev A.M. Phillippy E.E. Eichler StainedGlass: interactive visualization of massive tandem repeat structures with identity heatmaps Bioinformatics 2022 38 2049 2051 1:CAS:528:DC%2BB38XhtFygs7%2FK 35020798 8963321
A. Wallberg I. Bunikis O.V. Pettersson M.-B. Mosbech A.K. Childers J.D. Evans et al. A hybrid de novo genome assembly of the honeybee, Apis mellifera, with chromosome-length scaffolds BMC Genomics 2019 20 30961563 6454739
M.T. Webster A. Beaurepaire P. Neumann E. Stolle Population Genomics for Insect Conservation Annu Rev Anim Biosci 2022 6 e13095
P. Wlodzimierz M. Hong I.R. Henderson TRASH: Tandem Repeat Annotation and Structural Hierarchy Bioinformatics 2023 39 btad308 1:CAS:528:DC%2BB3sXhvVSrtrjL 37162382 10199239
D.E. Wood J. Lu B. Langmead Improved metagenomic analysis with Kraken 2 Genome Biol 2019 20 1:CAS:528:DC%2BC1MXitlynsbvJ 31779668 6883579
L.H. Yang C. Gratton Insects as drivers of ecosystem processes Curr Opin Insect Sci 2014 2 26 32 32846721
Y. Zhang J. Chu H. Cheng H. Li De novo reconstruction of satellite repeat units from sequence data Genome Res 2023 33 1994 2001 1:CAS:528:DC%2BB2cXit1GlsLvE 37918962 10760446
C. Zhou S.A. McCarthy R. Durbin YaHS: yet another Hi-C scaffolding tool Bioinformatics 2023 39 btac808 1:CAS:528:DC%2BB3sXhsFKisLbN 36525368
Y. Zhou Y. Wang X. Xiong A.G. Appel C. Zhang X. Wang Profiles of telomeric repeats in Insecta reveal diverse forms of telomeric motifs in Hymenopterans Life Sci Alliance 2022 5 202101163