Arsenophonus symbiosis with louse flies: multiple origins, coevolutionary dynamics, and metabolic significance

. 2023 Oct 26 ; 8 (5) : e0070623. [epub] 20230926

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37750682

Grantová podpora
20-07674S Grantová Agentura České Republiky (GAČR)

Insects that live exclusively on vertebrate blood utilize symbiotic bacteria as a source of essential compounds, e.g., B vitamins. In louse flies, the most frequent symbiont originated in genus Arsenophonus, known from a wide range of insects. Here, we analyze genomic traits, phylogenetic origins, and metabolic capacities of 11 Arsenophonus strains associated with louse flies. We show that in louse flies, Arsenophonus established symbiosis in at least four independent events, reaching different stages of symbiogenesis. This allowed for comparative genomic analysis, including convergence of metabolic capacities. The significance of the results is twofold. First, based on a comparison of independently originated Arsenophonus symbioses, it determines the importance of individual B vitamins for the insect host. This expands our theoretical insight into insect-bacteria symbiosis. The second outcome is of methodological significance. We show that the comparative approach reveals artifacts that would be difficult to identify based on a single-genome analysis.

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Baumann P. 2005. Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annu Rev Microbiol 59:155–189. doi:10.1146/annurev.micro.59.030804.121041 PubMed DOI

Moran NA. 1996. Accelerated evolution and Muller’s rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93:2873–2878. doi:10.1073/pnas.93.7.2873 PubMed DOI PMC

Bennett GM, Moran NA. 2015. Heritable Symbiosis: the advantages and perils of an evolutionary rabbit hole. Proc Natl Acad Sci U S A 112:10169–10176. doi:10.1073/pnas.1421388112 PubMed DOI PMC

Nováková E, Hypša V, Moran NA. 2009. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol 9:143. doi:10.1186/1471-2180-9-143 PubMed DOI PMC

Hypša V, Dale C. 1997. In vitro culture and phylogenetic analysis of "Candidatus Arsenophonus Triatominarum," an intracellular bacterium from the triatomine bug, Triatoma Infestans. Int J Syst Bacteriol 47:1140–1144. doi:10.1099/00207713-47-4-1140 PubMed DOI

Šorfová P, Škeříková A, Hypša V. 2008. An effect of 16S rRNA Intercistronic variability on coevolutionary analysis in symbiotic bacteria: molecular phylogeny of Arsenophonus triatominarum. Syst Appl Microbiol 31:88–100. doi:10.1016/j.syapm.2008.02.004 PubMed DOI

Rodríguez-Ruano SM, Škochová V, Rego ROM, Schmidt JO, Roachell W, Hypša V, Nováková E. 2018. Microbiomes of North American triatominae: the grounds for chagas disease epidemiology. Front Microbiol 9:1167. doi:10.3389/fmicb.2018.01167 PubMed DOI PMC

Hypša V. 1993. Endocytobionts of Triatoma Infestans – distribution and transmission. J Invertebr Pathol 61:32–38. doi:10.1006/jipa.1993.1006 DOI

Sasaki-Fukatsu K, Koga R, Nikoh N, Yoshizawa K, Kasai S, Mihara M, Kobayashi M, Tomita T, Fukatsu T. 2006. Symbiotic bacteria associated with stomach discs of human lice. Appl Environ Microbiol 72:7349–7352. doi:10.1128/AEM.01429-06 PubMed DOI PMC

Allen JM, Reed DL, Perotti MA, Braig HR. 2007. Evolutionary relationships of "Candidatus Riesia spp.," endosymbiotic enterobacteriaceae living within hematophagous primate lice. Appl Environ Microbiol 73:1659–1664. doi:10.1128/AEM.01877-06 PubMed DOI PMC

Šochová E, Husník F, Nováková E, Halajian A, Hypša V. 2017. Arsenophonus and Sodalis replacements shape evolution of symbiosis in louse flies. Peerj 5. doi:10.7717/peerj.4099 PubMed DOI PMC

Kutty SN, Pape T, Wiegmann BM, Meier R. 2010. Molecular phylogeny of the calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Syst Entomol 35:614–635. doi:10.1111/j.1365-3113.2010.00536.x DOI

Lehane MJ. 2005. The biology of blood-sucking in insects. 2nd ed. Cambridge University Press, Cambridge. doi:10.1017/CBO9780511610493 DOI

Douglas AE. 2017. The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Curr Opin Insect Sci 23:65–69. doi:10.1016/j.cois.2017.07.012 PubMed DOI

Nogge G. 1978. Aposymbiotic tsetse flies, Glossina Morsitans Moritans ontained by feeding on rabbits immunized specifically with symbionts. J Insect Physiol 24:299–304. doi:10.1016/0022-1910(78)90026-4 PubMed DOI

Baines S. 1956. The role of the symbiotic bacteria in the nutrition of Rhodnius prolixus (Hemiptera). J Exp Biol 33:533–541. doi:10.1242/jeb.33.3.533 DOI

Puchta O. 1955. Experimental investigations on the significance of symblotio organisms in P. humanus var. corporis. Zeitschrift fur Parasitenkunde 17:1–40. doi:10.1007/BF00260226 PubMed DOI

Boyd BM, Allen JM, de Crécy-Lagard V, Reed DL. 2014. Genome sequence of Candidatus Riesia pediculischaeffi, endosymbiont of chimpanzee lice, and genomic comparison of recently acquired endosymbionts from human and chimpanzee lice. G3 (Bethesda) 4:2189–2195. doi:10.1534/g3.114.012567 PubMed DOI PMC

Říhová J, Nováková E, Husník F, Hypša V. 2017. Legionella becoming a Mutualist: adaptive processes shaping the genome of Symbiont in the louse Polyplax serrata. Genome Biol Evol 9:2946–2957. doi:10.1093/gbe/evx217 PubMed DOI PMC

Rio RVM, Symula RE, Wang JW, Lohs C, Wu YN, Snyder AK, Bjornson RD, Oshima K, Biehl BS, Perna NT, Hattori M, Aksoy S. 2012. Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: glossinidae) obligate symbiont Wigglesworthia. Mbio 3:e00240-11. doi:10.1128/mBio.00240-11 PubMed DOI PMC

Nováková E, Husník F, Šochová E, Hypša V. 2015. Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl Environ Microbiol 81:6189–6199. doi:10.1128/AEM.01487-15 PubMed DOI PMC

Nováková E, Hypša V, Nguyen P, Husník F, Darby AC. 2016. Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae). Stand Genomic Sci 11:72. doi:10.1186/s40793-016-0195-1 PubMed DOI PMC

Říhová J, Bell KC, Nováková E, Hypša V. 2022. Lightella neohaematopini: a new lineage of highly reduced endosymbionts Coevolving with chipmunk lice of the genus neohaematopinus Front Microbiol 13:900312. doi:10.3389/fmicb.2022.900312 PubMed DOI PMC

Říhová J, Batani G, Rodríguez-Ruano SM, Martinů J, Vácha F, Nováková E, Hypša V. 2021. A new symbiotic lineage related to Neisseria and Snodgrassella arises from the dynamic and diverse microbiomes in sucking lice. Mol Ecol 30:2178–2196. doi:10.1111/mec.15866 PubMed DOI

Boyd BM, Allen JM, Nguyen N-P, Vachaspati P, Quicksall ZS, Warnow T, Mugisha L, Johnson KP, Reed DL. 2017. Primates, lice and bacteria: speciation and genome evolution in the Symbionts of hominid lice. Mol Biol Evol 34:1743–1757. doi:10.1093/molbev/msx117 PubMed DOI PMC

Andrews S. 2010. Fastqc: A quality control tool for high throughput sequence data. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. Spades: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. doi:10.1089/cmb.2012.0021 PubMed DOI PMC

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A. 2012. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. doi:10.1093/bioinformatics/bts199 PubMed DOI PMC

De Coster W, D’Hert S, Schultz DT, Cruts M, Van Broeckhoven C. 2018. Nanopack: visualizing and processing long-read sequencing data. Bioinformatics 34:2666–2669. doi:10.1093/bioinformatics/bty149 PubMed DOI PMC

Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. 2017. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27:722–736. doi:10.1101/gr.215087.116 PubMed DOI PMC

Li H. 2018. Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics 34:3094–3100. doi:10.1093/bioinformatics/bty191 PubMed DOI PMC

Vaser R, Sović I, Nagarajan N, Šikić M. 2017. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 27:737–746. doi:10.1101/gr.214270.116 PubMed DOI PMC

Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. doi:10.1093/bioinformatics/btu153 PubMed DOI

Emms DM, Kelly S. 2019. Orthofinder: phylogenetic orthology inference for comparative genomics. Genome Biol 20:238. doi:10.1186/s13059-019-1832-y PubMed DOI PMC

Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066. doi:10.1093/nar/gkf436 PubMed DOI PMC

Talavera G, Castresana J. 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. doi:10.1080/10635150701472164 PubMed DOI

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. doi:10.1093/sysbio/syq010 PubMed DOI

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R, Teeling E. 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534. doi:10.1093/molbev/msaa015 PubMed DOI PMC

Lartillot N, Rodrigue N, Stubbs D, Richer J. 2013. PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment. Syst Biol 62:611–615. doi:10.1093/sysbio/syt022 PubMed DOI

Lefort V, Longueville J-E, Gascuel O. 2017. SMS: smart model selection in PhyML. Mol Biol Evol 34:2422–2424. doi:10.1093/molbev/msx149 PubMed DOI PMC

Lartillot N, Brinkmann H, Philippe H. 2007. Suppression of long-branch attraction artefacts in the animal phylogeny using a site-heterogeneous model. BMC Evol Biol 7:S4. doi:10.1186/1471-2148-7-S1-S4 PubMed DOI PMC

Husník F, Chrudimský T, Hypša V. 2011. Multiple origins of endosymbiosis within the enterobacteriaceae (gamma-proteobacteria): convergence of complex phylogenetic approaches. BMC Biol. 9:87. doi:10.1186/1741-7007-9-87 PubMed DOI PMC

Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF. 2013. MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. doi:10.1016/j.ympev.2012.08.023 PubMed DOI

Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, Wishart DS. 2016. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44:W16–W21. doi:10.1093/nar/gkw387 PubMed DOI PMC

Syberg-Olsen MJ, Garber AI, Keeling PJ, McCutcheon JP, Husnik F. 2022. Pseudofinder: detection of pseudogenes in prokaryotic genomes. Mol Biol Evol 39:msac153. doi:10.1093/molbev/msac153 PubMed DOI PMC

Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain. PLoS One 5:e11147. doi:10.1371/journal.pone.0011147 PubMed DOI PMC

Gilchrist CLM, Chooi Y-H. 2021. Clinker & clustermap.Js: automatic generation of gene cluster comparison figures. Bioinformatics 37:2473–2475. doi:10.1093/bioinformatics/btab007 PubMed DOI

Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. 2016. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res 44:D457–62. doi:10.1093/nar/gkv1070 PubMed DOI PMC

Liu C, Cui Y, Li X, Yao M. 2021. Microeco: an R package for data mining in microbial community ecology. FEMS Microbiol Ecol 97:fiaa255. doi:10.1093/femsec/fiaa255 PubMed DOI

Ito K, Murphy D. 2013. Application of ggplot2 to pharmacometric graphics. CPT Pharmacometrics Syst Pharmacol 2:e79. doi:10.1038/psp.2013.56 PubMed DOI PMC

Bergsten J. 2005. A review of long-branch attraction. Cladistics 21:163–193. doi:10.1111/j.1096-0031.2005.00059.x PubMed DOI

Balmand S, Lohs C, Aksoy S, Heddi A. 2013. Tissue distribution and transmission routes for the tsetse fly endosymbionts. J Invertebr Pathol 112 Suppl:S116–22. doi:10.1016/j.jip.2012.04.002 PubMed DOI PMC

Tamas I, Klasson L, Canbäck B, Näslund AK, Eriksson A-S, Wernegreen JJ, Sandström JP, Moran NA, Andersson SGE. 2002. 50 million years of genomic stasis in endosymbiotic bacteria. Science 296:2376–2379. doi:10.1126/science.1071278 PubMed DOI

Wernegreen JJ. 2002. Genome evolution in bacterial endosymbionts of insects. Nat Rev Genet 3:850–861. doi:10.1038/nrg931 PubMed DOI

González-Domenech CM, Belda E, Patiño-Navarrete R, Moya A, Peretó J, Latorre A. 2012. Metabolic stasis in an ancient symbiosis: genome-scale metabolic networks from two blattabacterium cuenoti strains, primary endosymbionts of cockroaches. BMC Microbiol 12 Suppl 1:S5. doi:10.1186/1471-2180-12-S1-S5 PubMed DOI PMC

Sloan DB, Moran NA. 2013. The evolution of genomic instability in the obligate endosymbionts of whiteflies. Genome Biol Evol 5:783–793. doi:10.1093/gbe/evt044 PubMed DOI PMC

Soucy SM, Huang J, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat Rev Genet 16:472–482. doi:10.1038/nrg3962 PubMed DOI

Moran NA. 2003. Tracing the evolution of gene loss in obligate bacterial symbionts. Curr Opin Microbiol 6:512–518. doi:10.1016/j.mib.2003.08.001 PubMed DOI

Martinez-Gomez NC, Palmer LD, Vivas E, Roach PL, Downs DM. 2011. The Rhodanese domain of thiI is both necessary and sufficient for synthesis of the thiazole moiety of thiamine in Salmonella enterica. J Bacteriol 193:4582–4587. doi:10.1128/JB.05325-11 PubMed DOI PMC

Lu S, Wang J, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS, Thanki N, Yamashita RA, Yang M, Zhang D, Zheng C, Lanczycki CJ, Marchler-Bauer A. 2020. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48:D265–D268. doi:10.1093/nar/gkz991 PubMed DOI PMC

Snyder AK, McLain C, Rio RVM. 2012. The Tsetse fly obligate mutualist Wigglesworthia morsitans alters gene expression and population density via exogenous nutrient provisioning. Appl Environ Microbiol 78:7792–7797. doi:10.1128/AEM.02052-12 PubMed DOI PMC

Kenyon LJ, Meulia T, Sabree ZL. 2015. Habitat visualization and genomic analysis of "Candidatus Pantoea carbekii," the primary symbiont of the brown marmorated stink bug. Genome Biol Evol 7:620–635. doi:10.1093/gbe/evv006 PubMed DOI PMC

Gilliland CA, Patel V, McCormick AC, Mackett BM, Vogel KJ. 2023. Using axenic and gnotobiotic insects to examine the role of different microbes on the development and reproduction of the kissing bug Rhodnius prolixus (Hemiptera: Reduviidae). Mol Ecol 32:920–935. doi:10.1111/mec.16800 PubMed DOI PMC

Santos-Garcia D, Juravel K, Freilich S, Zchori-Fein E, Latorre A, Moya A, Morin S, Silva FJ. 2018. To B or not to B: comparative genomics suggests Arsenophonus as a source of B vitamins in whiteflies. Front Microbiol 9:2254. doi:10.3389/fmicb.2018.02254 PubMed DOI PMC

Husnik F, Hypsa V, Darby A, Cordaux RT. 2020. Insect-symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite. Genome Biol and Evol 12:429–442. doi:10.1093/gbe/evaa032 PubMed DOI PMC

Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, Lee SH, Robertson HM, Kennedy RC, Elhaik E, Gerlach D, Kriventseva EV, Elsik CG, Graur D, Hill CA, Veenstra JA, Walenz B, Tubío JMC, Ribeiro JMC, Rozas J, Johnston JS, Reese JT, Popadic A, Tojo M, Raoult D, Reed DL, Tomoyasu Y, Kraus E, Mittapalli O, Margam VM, Li H-M, Meyer JM, Johnson RM, Romero-Severson J, Vanzee JP, Alvarez-Ponce D, Vieira FG, Aguadé M, Guirao-Rico S, Anzola JM, Yoon KS, Strycharz JP, Unger MF, Christley S, Lobo NF, Seufferheld MJ, Wang N, Dasch GA, Struchiner CJ, Madey G, Hannick LI, Bidwell S, Joardar V, Caler E, Shao R, Barker SC, Cameron S, Bruggner RV, Regier A, Johnson J, Viswanathan L, Utterback TR, Sutton GG, Lawson D, Waterhouse RM, Venter JC, Strausberg RL, Berenbaum MR, Collins FH, Zdobnov EM, Pittendrigh BR. 2010. Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci U S A 107:12168–12173. doi:10.1073/pnas.1003379107 PubMed DOI PMC

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

Chrudimský T, Husník F, Nováková E, Hypša V. 2012. Candidatus Sodalis melophagi sp nov.: phylogenetically independent comparative model to the tsetse fly symbiont Sodalis glossinidius. PLoS One 7:e40354. doi:10.1371/journal.pone.0040354 PubMed DOI PMC

Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout Mutants: the keio collection. Mol Syst Biol 2:2006. doi:10.1038/msb4100050 PubMed DOI PMC

Haase I, Sarge S, Illarionov B, Laudert D, Hohmann H-P, Bacher A, Fischer M. 2013. Enzymes from the haloacid dehalogenase (HAD) superfamily catalyse the elusive dephosphorylation step of riboflavin biosynthesis. Chembiochem 14:2272–2275. doi:10.1002/cbic.201300544 PubMed DOI

Liu S, Hu W, Wang Z, Chen T. 2020. Production of riboflavin and related cofactors by biotechnological processes. Microb Cell Fact 19:31. doi:10.1186/s12934-020-01302-7 PubMed DOI PMC

Richts B, Commichau FM. 2021. Underground metabolism facilitates the evolution of novel pathways for vitamin B6 biosynthesis. Appl Microbiol Biotechnol 105:2297–2305. doi:10.1007/s00253-021-11199-w PubMed DOI PMC

Tramonti A, Nardella C, de Salvo ML, Barile A, D’Alessio F, de Crécy-Lagard V, Contestabile R. 2021. Knowns and unknowns of vitamin B(6) metabolism in Escherichia Coli. EcoSal Plus 9:1128. doi:10.1128/ecosalplus.ESP-0004-2021 PubMed DOI PMC

Price DRG, Wilson ACC. 2014. A substrate ambiguous enzyme facilitates genome reduction in an intracellular symbiont. BMC Biol. 12:110. doi:10.1186/s12915-014-0110-4 PubMed DOI PMC

Hazra AB, Han Y, Chatterjee A, Zhang Y, Lai R-Y, Ealick SE, Begley TP. 2011. A missing enzyme in thiamin thiazole biosynthesis: identification of Teni as a thiazole tautomerase. J Am Chem Soc 133:9311–9319. doi:10.1021/ja1110514 PubMed DOI PMC

Li K, Li T, Yang S-S, Wang X-D, Gao L-X, Wang R-Q, Gu J, Zhang X-E, Deng J-Y. 2017. Deletion of nudB causes increased susceptibility to antifolates in Escherichia coli and Salmonella enterica. Antimicrob Agents Chemother 61:e02378-16. doi:10.1128/AAC.02378-16 PubMed DOI PMC

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