Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae)
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu kazuistiky, časopisecké články
PubMed
27660670
PubMed Central
PMC5027103
DOI
10.1186/s40793-016-0195-1
PII: 195
Knihovny.cz E-zdroje
- Klíčová slova
- Arsenophonus, Hippoboscidae, Symbiosis, Tsetse,
- Publikační typ
- časopisecké články MeSH
- kazuistiky MeSH
Candidatus Arsenophonus lipopteni (Enterobacteriaceae, Gammaproteobacteria) is an obligate intracellular symbiont of the blood feeding deer ked, Lipoptena cervi (Diptera: Hippoboscidae). The bacteria reside in specialized cells derived from host gut epithelia (bacteriocytes) forming a compact symbiotic organ (bacteriome). Compared to the closely related complex symbiotic system in the sheep ked, involving four bacterial species, Lipoptena cervi appears to maintain its symbiosis exclusively with Ca. Arsenophonus lipopteni. The genome of 836,724 bp and 24.8 % GC content codes for 667 predicted functional genes and bears the common characteristics of sequence economization coupled with obligate host-dependent lifestyle, e.g. reduced number of RNA genes along with the rRNA operon split, and strongly reduced metabolic capacity. Particularly, biosynthetic capacity for B vitamins possibly supplementing the host diet is highly compromised in Ca. Arsenophonus lipopteni. The gene sets are complete only for riboflavin (B2), pyridoxine (B6) and biotin (B7) implying the content of some B vitamins, e.g. thiamin, in the deer blood might be sufficient for the insect metabolic needs. The phylogenetic position within the spectrum of known Arsenophonus genomes and fundamental genomic features of Ca. Arsenophonus lipopteni indicate the obligate character of this symbiosis and its independent origin within Hippoboscidae.
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Beard CB, Cordon-Rosales C, Durvasula RV. Bacterial Symbionts of the Triatominae and their potential use in control of Chagas disease transmission 1. Annu Rev Entomol. 2002;47:123–141. doi: 10.1146/annurev.ento.47.091201.145144. PubMed DOI
Gumiel M, da Mota FF, Rizzo Vde S, Sarquis O, de Castro DP, Lima MM, et al. Characterization of the microbiota in the guts of Triatoma brasiliensis and Triatoma pseudomaculata infected by Trypanosoma cruzi in natural conditions using culture independent methods. Parasit Vectors. 2015;8:245. doi: 10.1186/s13071-015-0836-z. PubMed DOI PMC
Hypša V, Křížek J. Molecular evidence for polyphyletic origin of the primary symbionts of sucking lice (Phthiraptera, Anoplura) Microbial Ecol. 2007;54:242–251. doi: 10.1007/s00248-006-9194-x. PubMed DOI
Sasaki-Fukatsu K, Koga R, Nikoh N, Yoshizawa K, Kasai S, Mihara M, et al. Symbiotic bacteria associated with stomach discs of human lice. Appl Environ Microbiol. 2006;72:7349–7352. doi: 10.1128/AEM.01429-06. PubMed DOI PMC
Hosokawa T, Koga R, Kikuchi Y, Meng XY, Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A. 2010;107:769–774. doi: 10.1073/pnas.0911476107. PubMed DOI PMC
Aksoy S, Chen X, Hypsa V. Phylogeny and potential transmission routes of midgut-associated endosymbionts of tsetse (Diptera: Glossinidae) Insect Mol Biol. 1997;6:183–190. doi: 10.1111/j.1365-2583.1997.tb00086.x. PubMed DOI
Nováková E, Husník F, Šochová E, Hypša V. Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Appl Environ Microbiol. 2015;81:6189–6199. doi: 10.1128/AEM.01487-15. PubMed DOI PMC
Nelson M, Graf J. Bacterial symbioses of the medicinal leech Hirudo verbana. Gut Microbes. 2012;3:322–331. doi: 10.4161/gmic.20227. PubMed DOI PMC
Manzano-Marín A, Oceguera-Figueroa A, Latorre A, Jiménez-García LF, Moya A. Solving a bloody mess: B-vitamin independent metabolic convergence among gammaproteobacterial obligate endosymbionts from blood-feeding arthropods and the leech Haementeria officinalis. Gen Biol Evol. 2015;7:2871–2884. doi: 10.1093/gbe/evv188. PubMed DOI PMC
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990;56:1919–1925. PubMed PMC
Behrens S, Rühland C, Inácio J, Huber H, Fonseca A, Spencer-Martins I, et al. In situ accessibility of small-subunit rRNA of members of the domains Bacteria, Archaea, and Eucarya to Cy3-labeled oligonucleotide probes. App Environ Microbiol. 2003;69:1748–1758. doi: 10.1128/AEM.69.3.1748-1758.2003. PubMed DOI PMC
Charles H, Heddi A, Rahbe Y. A putative insect intracellular endosymbiont stem clade, within the Enterobacteriaceae, inferred from phylogenetic analysis based on a heterogeneous model of DNA evolution. C R Acad Sci Ser III Sci Vie. 2001;324:489–494. doi: 10.1016/S0764-4469(01)01328-2. PubMed DOI
Dehal PS, Joachimiak MP, Price MN, Bates JT, Baumohl JK, Chivian D, et al. MicrobesOnline: an integrated portal for comparative and functional genomics. Nucleic Acids Res. 2010;38:D396–D400. doi: 10.1093/nar/gkp919. PubMed DOI PMC
Lerat E, Daubin V, Moran NA. From gene trees to organismal phylogeny in prokaryotes: the case of the γ-proteobacteria. PLoS Biol. 2003;1:e19. doi: 10.1371/journal.pbio.0000019. PubMed DOI PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Lartillot N, Lepage T, Blanquart S. PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics. 2009;25:2286–2288. doi: 10.1093/bioinformatics/btp368. PubMed DOI
Nováková E, Hypša V, Moran NA. Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiol. 2009;9:1–14. doi: 10.1186/1471-2180-9-143. PubMed DOI PMC
Tritt A, Eisen JA, Facciotti MT, Darling AE. An integrated pipeline for de novo assembly of microbial genomes. PLoS One. 2012;7:e42304. doi: 10.1371/journal.pone.0042304. PubMed DOI PMC
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, et al. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One. 2014;9:e112963. doi: 10.1371/journal.pone.0112963. PubMed DOI PMC
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genomics. 2008;9:75. doi: 10.1186/1471-2164-9-75. PubMed DOI PMC
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI
Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28:33–36. doi: 10.1093/nar/28.1.33. PubMed DOI PMC
Petersen TN, Brunak S, von Heijne G, Nielsen H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods. 2011;8:785–786. doi: 10.1038/nmeth.1701. PubMed DOI
Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol. 2011;7:e1002195. doi: 10.1371/journal.pcbi.1002195. PubMed DOI PMC
Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, et al. The Pfam protein families database. Nucleic Acids Res. 2002;30:276–280. doi: 10.1093/nar/30.1.276. PubMed DOI PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–1649. doi: 10.1093/bioinformatics/bts199. PubMed DOI PMC
McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 2012;10:13–26. PubMed
Merhej V, Royer-Carenzi M, Pontarotti P, Raoult D. Massive comparative genomic analysis reveals convergent evolution of specialized bacteria. Biol Direct. 2009;4:13. doi: 10.1186/1745-6150-4-13. PubMed DOI PMC
Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM, et al. 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. 2010;107:12168–12173. doi: 10.1073/pnas.1003379107. PubMed DOI PMC
Attardo GM, Abila PP, Auma JE, Baumann AA, Benoit JB, Brelsfoard CL, et al. Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science. 2014;344:380–386. doi: 10.1126/science.1249656. PubMed DOI PMC
Jaehme M, Slotboom DJ. Diversity of membrane transport proteins for vitamins in bacteria and archaea. Biochimica et Biophysica Acta (BBA)-General Subjects. 2015;1850:565–576. doi: 10.1016/j.bbagen.2014.05.006. PubMed DOI
Puchta O. Experimentelle Untersuchungen über die Bedeutung der Symbiose der Kleiderlaus Pediculus vestimenti Burm. Z Parasitenkd. 1955;17:1–40. doi: 10.1007/BF00260226. PubMed DOI
Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–4579. doi: 10.1073/pnas.87.12.4576. PubMed DOI PMC
Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. Volume 2, Part B. 2. New York: Springer; 2005. p. 1.
Garrity GM, Bell JA, Lilburn T. Class III. Gammaproteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, vol. Volume 2, Part B. 2. New York: Springer; 2005. p. 1.
Garrity GM, Holt JG. Taxonomic Outline of the Archaea and Bacteria. In: Garrity GM, Boone DR, Castenholz RW, editors. Bergey’s Manual of Systematic Bacteriology, vol. Volume 1. 2. New York: Springer; 2001. pp. 155–166.
Judicial Commission Conservation of the family name Enterobacteriaceae, of the name of the type genus, and designation of the type species OPINION NO. 15. Int Bull Bacteriol Nomencl Taxon. 1958;8:73–4.
Werren JH. Arsenophonus. Bergey’s Manual of Systematic Bacteriology (Vol. 2), G.M. Garrity (ed), New York: Springer-Verlag; 2004:1–4
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25:25–29. doi: 10.1038/75556. PubMed DOI PMC
Insect-Symbiont Gene Expression in the Midgut Bacteriocytes of a Blood-Sucking Parasite
Microbiomes of North American Triatominae: The Grounds for Chagas Disease Epidemiology
Arsenophonus and Sodalis replacements shape evolution of symbiosis in louse flies