The phylogenetic diversity of symbiotic bacteria in sucking lice suggests that lice have a complex history of symbiont acquisition, loss, and replacement throughout their evolution. These processes have resulted in the establishment of different, phylogenetically distant bacteria as obligate mutualists in different louse groups. By combining metagenomics and amplicon screening across several populations of three louse species (members of the genera Polyplax and Hoplopleura) we describe a novel louse symbiont lineage related to Neisseria and Snodgrassella, and show its independent origin in the two louse genera. While the genomes of these symbionts are highly similar, their respective distributions and status within lice microbiomes indicate that they have different functions and history. In Hoplopleura acanthopus, the Neisseriaceae-related bacterium is a dominant obligate symbiont present across several host populations. In contrast, the Polyplax microbiomes are dominated by the obligate symbiont Legionella polyplacis, with the Neisseriaceae-related bacterium co-occurring only in some samples and with much lower abundance. The results thus support the view that compared to other exclusively blood feeding insects, Anoplura possess a unique capacity to acquire symbionts from diverse groups of bacteria.

Department of Chemistry Faculty of Science University of South Bohemia České Budějovice Czech Republic

Department of Parasitology Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Parasitology Biology Centre ASCR v v i České Budějovice Czech Republic

Zobrazit více v PubMed

Ahantarig, A., Trinachartvanit, W., Baimai, V., & Grubhoffer, L. (2013). Hard ticks and their bacterial endosymbionts (or would be pathogens). Folia Microbiologica, 58(5), 419-428. https://doi.org/10.1007/s12223-013-0222-1

Aksoy, S. (2000). Tsetse - A haven for microorganisms. Parasitology Today, 16(3), 114-118. https://doi.org/10.1016/S0169-4758(99)01606-3

Allen, J. M., Burleigh, J. G., Light, J. E., & Reed, D. L. (2016). Effects of 16S rDNA sampling on estimates of the number of endosymbiont lineages in sucking lice. PeerJ, 4, e2187. https://doi.org/10.7717/peerj.2187

Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215(3), 403-410. https://doi.org/10.1016/S0022-2836(05)80360-2

Amann, R., Krumholz, L., & Stahl, D. (1990). Fluorescent-oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. Journal of Bacteriology, 172(2), 762-770. https://doi.org/10.1128/jb.172.2.762-770.1990

Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. Retrieved from http://www.bioinformatics.babraham.ac.uk/projects/fastqc

Apprill, A., McNally, S., Parsons, R., & Weber, L. (2015). Minor revision to V4 region SSU rRNA 806R gene primer greatly increases detection of SAR11 bacterioplankton. Aquatic Microbial Ecology, 75(2), 129-137. https://doi.org/10.3354/ame01753

Aziz, R. K., Bartels, D., Best, A. A., DeJongh, M., Disz, T., Edwards, R. A., Formsma, K., Gerdes, S., Glass, E. M., Kubal, M., Meyer, F., Olsen, G. J., Olson, R., Osterman, A. L., Overbeek, R. A., McNeil, L. K., Paarmann, D., Paczian, T., Parrello, B., … Zagnitko, O. (2008). The RAST Server: Rapid annotations using subsystems technology. BMC Genomics, 9(1), 75. https://doi.org/10.1186/1471-2164-9-75

Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19(5), 455-477. https://doi.org/10.1089/cmb.2012.0021

Baumann, P. (2005). Biology of bacteriocyte-associated endosymbionts of plant sap-sucking insects. Annual Review of Microbiology, 59, 155-189. https://doi.org/10.1146/annurev.micro.59.030804.121041

Bennett, G. M., & Moran, N. A. (2013). Small, smaller, smallest: The origins and evolution of ancient dual symbioses in a phloem-feeding insect. Genome Biology and Evolution, 5(9), 1675-1688. https://doi.org/10.1093/gbe/evt118

Bennett, G. M., & Moran, N. A. (2015). Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole. Proceedings of the National Academy of Sciences of the United States of America, 112(33), 10169-10176. https://doi.org/10.1073/pnas.1421388112

Bokulich, N. A., Subramanian, S., Faith, J. J., Gevers, D., Gordon, J. I., Knight, R., Mills, D. A., & Caporaso, J. G. (2013). Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nature Methods, 10(1), 57-59. https://doi.org/10.1038/nmeth.2276

Boyd, B. M., Allen, J. M., de Crécy-Lagard, V., & Reed, D. L. (2014). Genome sequence of Candidatus Riesia pediculischaeffi, endosymbiont of chimpanzee lice, and genomic comparison of recently acquired endosymbionts from human and chimpanzee lice. G3: Genes, Genomes, Genetics, 4(11), 2189-2195. https://doi.org/10.1534/g3.114.012567

Boyd, B. M., Allen, J. M., Koga, R., Fukatsu, T., Sweet, A. D., Johnson, K. P., & Reed, D. L. (2016). Two bacterial genera, Sodalis and Rickettsia, associated with the seal louse Proechinophthirus fluctus (Phthiraptera: Anoplura). Applied and Environmental Microbiology, 82(11), 3185-3197. https://doi.org/10.1128/AEM.00282-16

Boyd, B. M., Allen, J. M., Nguyen, N.-P., Vachaspati, P., Quicksall, Z. S., Warnow, T., Mugisha, L., Johnson, K. P., & Reed, D. L. (2017). Primates, lice and bacteria: Speciation and genome evolution in the symbionts of hominid lice. Molecular Biology and Evolution, 34(7), 1743-1757. https://doi.org/10.1093/molbev/msx117

Brewer, T. E., Albertsen, M., Edwards, A., Kirkegaard, R. H., Rocha, E. P., & Fierer, N. (2020). Unlinked rRNA genes are widespread among bacteria and archaea. The ISME Journal, 14(2), 597-608. https://doi.org/10.1038/s41396-019-0552-3

Brown, J. J., Rodríguez-Ruano, S. M., Poosakkannu, A., Batani, G., Schmidt, J. O., Roachell, W., Zima, J., Hypša, V., & Nováková, E. (2020). Ontogeny, species identity and environment dominate microbiome dynamics in wild populations of kissing bugs (Triatominae). Microbiome, 8, 146. https://doi.org/10.1186/s40168-020-00921-x

Bushnell, B. (2014). BBMap: A fast, accurate, splice-aware aligner (No. LBNL-7065E). Lawrence Berkeley National Laboratory, Berkeley.

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics, 10(1), 421. https://doi.org/10.1186/1471-2105-10-421

Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Peña, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335. https://doi.org/10.1038/nmeth.f.303

Carattoli, A., Zankari, E., García-Fernández, A., Larsen, M. V., Lund, O., Villa, L., & Hasman, H. (2014). In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58(7), 3895-3903. https://doi.org/10.1128/AAC.02412-14

Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 540-552. https://doi.org/10.1093/oxfordjournals.molbev.a026334

Chen, X., Li, S., & Aksoy, S. (1999). Concordant evolution of a symbiont with its host insect species: Molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. Journal of Molecular Evolution, 48(1), 49-58. https://doi.org/10.1007/PL00006444

Darling, A. E., Mau, B., & Perna, N. T. (2010). progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLoS One, 5(6), e11147. https://doi.org/10.1371/journal.pone.0011147

Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772. https://doi.org/10.1038/nmeth.2109

De Coster, W., D’Hert, S., Schultz, D. T., Cruts, M., & Van Broeckhoven, C. (2018). NanoPack: Visualizing and processing long-read sequencing data. Bioinformatics, 34(15), 2666-2669. https://doi.org/10.1093/bioinformatics/bty149

Demchenko, A. P. (2020). Photobleaching of organic fluorophores: Quantitative characterization, mechanisms, protection. Methods and Applications in Fluorescence, 8(2), 022001. https://doi.org/10.1088/2050-6120/ab7365

Dhami, M. K., Buckley, T. R., Beggs, J. R., & Taylor, M. W. (2013). Primary symbiont of the ancient scale insect family Coelostomidiidae exhibits strict cophylogenetic patterns. Symbiosis, 61(2), 77-91. https://doi.org/10.1007/s13199-013-0257-8

Dick, C. W. (2006). Checklist of world Hippoboscidae (Diptera: Hippoboscoidea) (pp. 1-7). Department of Zoology, Field Museum Natural History.

Doudoumis, V., Blow, F., Saridaki, A., Augustinos, A., Dyer, N. A., Goodhead, I., Solano, P., Rayaisse, J.-B., Takac, P., Mekonnen, S., Parker, A. G., Abd-Alla, A. M. M., Darby, A., Bourtzis, K., & Tsiamis, G. (2017). Challenging the Wigglesworthia, Sodalis, Wolbachia symbiosis dogma in tsetse flies: Spiroplasma is present in both laboratory and natural populations. Scientific Reports, 7(1), 1-13. https://doi.org/10.1038/s41598-017-04740-3

Douglas, A. E. (2015). Multiorganismal insects: Diversity and function of resident microorganisms. Annual Review of Entomology, 60, 17-34. https://doi.org/10.1146/annurev-ento-010814-020822

Edgar, R. C. (2013). UPARSE: Highly accurate OTU sequences from microbial amplicon reads. Nature Methods, 10(10), 996. https://doi.org/10.1038/nmeth.2604

Eggeling, C., Widengren, J., Rigler, R., & Seidel, C. A. M. (1998). Photobleaching of fluorescent dyes under conditions used for single-molecule detection: Evidence of two-step photolysis. Analytical Chemistry, 70(13), 2651-2659. https://doi.org/10.1021/ac980027p

Emms, D. M., & Kelly, S. (2019). OrthoFinder: Phylogenetic orthology inference for comparative genomics. Genome Biology, 20(1), 1-14. https://doi.org/10.1186/s13059-019-1832-y

Engel, P., & Moran, N. A. (2013). The gut microbiota of insects-diversity in structure and function. FEMS Microbiology Reviews, 37(5), 699-735. https://doi.org/10.1111/1574-6976.12025

Felsheim, R. F., Kurtti, T. J., & Munderloh, U. G. (2009). Genome sequence of the endosymbiont Rickettsia peacockii and comparison with virulent Rickettsia rickettsii: Identification of virulence factors. PLoS One, 4(12), e8361. https://doi.org/10.1371/journal.pone.0008361

Folmer, O., Black, M., Hoeh, W., Lutz, R., & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3(5), 294-299. https://doi.org/10.1128/AEM.00226-09

Fukatsu, T., Hosokawa, T., Koga, R., Nikoh, N., Kato, T., Hayama, S.-I., Takefushi, H., & Tanaka, I. (2009). Intestinal endocellular symbiotic bacterium of the macaque louse Pedicinus obtusus: Distinct endosymbiont origins in anthropoid primate lice and the old world monkey louse. Applied Environmental Microbiology, 75(11), 3796-3799. https://doi.org/10.1128/AEM.00226-09

Gauthier, J. P., Outreman, Y., Mieuzet, L., & Simon, J. C. (2015). Bacterial communities associated with host-adapted populations of pea aphids revealed by deep sequencing of 16S ribosomal DNA. PLoS One, 10(3), e0120664. https://doi.org/10.1371/journal.pone.0120664

Gerhart, J. G., Moses, A. S., & Raghavan, R. (2016). A Francisella-like endosymbiont in the Gulf Coast tick evolved from a mammalian pathogen. Scientific Reports, 6, 33670. https://doi.org/10.1038/srep33670

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. Systematic Biology, 59(3), 307-321. https://doi.org/10.1093/sysbio/syq010

Guindon, S., & Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52(5), 696-704. https://doi.org/10.1080/10635150390235520

Guizzo, M. G., Parizi, L. F., Nunes, R. D., Schama, R., Albano, R. M., Tirloni, L., Oldiges, D. P., Vieira, R. P., Oliveira, W. H. C., Leite, M. D. S., Gonzales, S. A., Farber, M., Martins, O., Vaz, I. D. S., & Oliveira, P. L. (2017). A Coxiella mutualist symbiont is essential to the development of Rhipicephalus microplus. Scientific Reports, 7(1), 1-10. https://doi.org/10.1038/s41598-017-17309-x

Hafner, M. S., Sudman, P. D., Villablanca, F. X., Spradling, T. A., Demastes, J. W., & Nadler, S. A. (1994). Disparate rates of molecular evolution in cospeciating hosts and parasites. Science, 265(5175), 1087-1090. https://doi.org/10.1126/science.8066445

Hosokawa, T., Nikoh, N., Koga, R., Satô, M., Tanahashi, M., Meng, X. Y., & Fukatsu, T. (2012). Reductive genome evolution, host-symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies. The ISME Journal, 6(3), 577-587. https://doi.org/10.1038/ismej.2011.125

Husnik, F., Nikoh, N., Koga, R., Ross, L., Duncan, R. P., Fujie, M., Tanaka, M., Satoh, N., Bachtrog, D., Wilson, A. C. C., von Dohlen, C. D., Fukatsu, T., & McCutcheon, J. P. (2013). Horizontal gene transfer from diverse bacteria to an insect genome enables a tripartite nested mealybug symbiosis. Cell, 153(7), 1567-1578. https://doi.org/10.1016/j.cell.2013.05.040

Hypša, V., & Křížek, J. (2007). Molecular evidence for polyphyletic origin of the primary symbionts of sucking lice (Phthiraptera, Anoplura). Microbial Ecology, 54(2), 242-251. https://doi.org/10.1007/s00248-006-9194-x

Jones, R. T., McCormick, K. F., & Martin, A. P. (2008). Bacterial communities of Bartonella-positive fleas: Diversity and community assembly patterns. Applied and Environmental Microbiology, 74(5), 1667-1670. https://doi.org/10.1128/AEM.02090-07

Kanehisa, M., Sato, Y., Kawashima, M., Furumichi, M., & Tanabe, M. (2016). KEGG as a reference resource for gene and protein annotation. Nucleic Acids Research, 44(D1), D457-D462. https://doi.org/10.1093/nar/gkv1070

Katoh, K., Misawa, K., Kuma, K. I., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059-3066. https://doi.org/10.1093/nar/gkf436

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(12), 1647-1649. https://doi.org/10.1093/bioinformatics/bts199

Kirkness, E. F., Haas, B. J., Sun, W., Braig, H. R., Perotti, M. A., Clark, J. M., Lee, S. H., Robertson, H. M., Kennedy, R. C., Elhaik, E., Gerlach, D., Kriventseva, E. V., Elsik, C. G., Graur, D., Hill, C. A., Veenstra, J. A., Walenz, B., Tubio, J. M. C., Ribeiro, J. M. C., … Pittendrigh, B. R. (2010). Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proceedings of the National Academy of Sciences, 107(27), 12168-12173. https://doi.org/10.1073/pnas.1003379107

Klein, A., Schrader, L., Gil, R., Manzano-Marín, A., Flórez, L., Wheeler, D., Werren, J. H., Latorre, A., Heinze, J., Kaltenpoth, M., Moya, A., & Oettler, J. (2016). A novel intracellular mutualistic bacterium in the invasive ant Cardiocondyla obscurior. The ISME Journal, 10(2), 376-388. https://doi.org/10.1038/ismej.2015.119

Kolmogorov, M., Yuan, J., Lin, Y., & Pevzner, P. A. (2019). Assembly of long, error-prone reads using repeat graphs. Nature Biotechnology, 37(5), 540-546. https://doi.org/10.1038/s41587-019-0072-8

Koren, S., Walenz, B. P., Berlin, K., Miller, J. R., Bergman, N. H., & Phillippy, A. M. (2017). Canu: Scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Research, 27(5), 722-736. https://doi.org/10.1101/gr.215087.116.

Kwong, W. K., & Moran, N. A. (2013). Cultivation and characterization of the gut symbionts of honey bees and bumble bees: Description of Snodgrassella alvi gen. nov., sp. nov., a member of the family Neisseriaceae of the Betaproteobacteria, and Gilliamella apicola gen. nov., sp. nov., a member of Orbaceae fam. nov., Orbales ord. nov., a sister taxon to the order ‘Enterobacteriales’ of the Gammaproteobacteria. International Journal of Systematic and Evolutionary Microbiology, 63(6), 2008-2018. https://doi.org/10.1099/ijs.0.044875-0

Laetsch, D. R., & Blaxter, M. L. (2017). BlobTools: Interrogation of genome assemblies. F1000Research, 6, 1287. https://doi.org/10.12688/f1000research.12232.1

Lefort, V., Longueville, J. E., & Gascuel, O. (2017). SMS: Smart model selection in PhyML. Molecular Biology and Evolution, 34(9), 2422-2424. https://doi.org/10.1093/molbev/msx149

Leinonen, R., Sugawara, H., & Shumway, M. (2011). The sequence read archive. Nucleic Acids Research, 39, D19-D21. https://doi.org/10.1093/nar/gkq1019

Li, H. (2018). Minimap2: Pairwise alignment for nucleotide sequences. Bioinformatics, 34(18), 3094-3100. https://doi.org/10.1093/bioinformatics/bty191

Light, J. E., Smith, V. S., Allen, J. M., Durden, L. A., & Reed, D. L. (2010). Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura). BMC Evolutionary Biology, 10(1), 292. https://doi.org/10.1186/1471-2148-10-292

Mahmoudian, J., Hadavi, R., Jeddi-Tehrani, M., Mahmoudi, A. R., Bayat, A. A., Shaban, E., & Ghods, R. (2011). Comparison of the photobleaching and photostability traits of Alexa Fluor 568- and fluorescein isothiocyanate- conjugated antibody. Cell Journal, 13(3), 169-172.

Manzano-Marı́n, A., Coeur d’acier, A., Clamens, A.-L., Orvain, C., Cruaud, C., Barbe, V., & Jousselin, E. (2020). Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids’ di-symbiotic systems. The ISME Journal, 14(1), 259-273. https://doi.org/10.1038/s41396-019-0533-6

Manzano-Marín, A., Szabó, G., Simon, J. C., Horn, M., & Latorre, A. (2017). Happens in the best of subfamilies: Establishment and repeated replacements of co-obligate secondary endosymbionts within Lachninae aphids. Environmental Microbiology, 19(1), 393-408. https://doi.org/10.1111/1462-2920.13633

Martinson, V. G., Moy, J., & Moran, N. A. (2012). Establishment of characteristic gut bacteria during development of the honeybee worker. Applied and Environmental Microbiology, 78(8), 2830-2840. https://doi.org/10.1128/AEM.07810-11

Martinů, J., Hypša, V., & Štefka, J. (2018). Host specificity driving genetic structure and diversity in ectoparasite populations: Coevolutionary patterns in Apodemus mice and their lice. Ecology and Evolution, 8(20), 10008-10022. https://doi.org/10.1002/ece3.4424

McCutcheon, J. P., Boyd, B. M., & Dale, C. (2019). The life of an insect endosymbiont from the cradle to the grave. Current Biology, 29(11), 485-495. https://doi.org/10.1016/j.cub.2019.03.032

Meseguer, A. S., Manzano-Marín, A., Coeur D'Acier, A., Clamens, A. L., Godefroid, M., & Jousselin, E. (2017). Buchnera has changed flatmate but the repeated replacement of co-obligate symbionts is not associated with the ecological expansions of their aphid hosts. Molecular Ecology, 26(8), 2363-2378. https://doi.org/10.1111/mec.13910

Moran, N. A. (1996). Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proceedings of the National Academy of Sciences, 93(7), 2873-2878. https://doi.org/10.1073/pnas.93.7.2873

Moran, N. A., Munson, M. A., Baumann, P., & Ishikawa, H. (1993). A molecular clock in endosymbiotic bacteria is calibrated using the insect hosts. Proceedings of the Royal Society of London, Series B: Biological Sciences, 253(1337), 167-171. https://doi.org/10.1098/rspb.1993.0098

Munson, M. A., Baumann, L., & Baumann, P. (1993). Buchnera aphidicola (a prokaryotic endosymbiont of aphids) contains a putative 16S rRNA operon unlinked to the 23S rRNA-encoding gene: Sequence determination, and promoter and terminator analysis. Gene, 137(2), 171-178. https://doi.org/10.1016/0378-1119(93)90003-L

Niebylski, M. L., Peacock, M. G., Fischer, E. R., Porcella, S. F., & Schwan, T. G. (1997). Characterization of an endosymbiont infecting wood ticks, Dermacentor andersoni, as a member of the genus Francisella. Applied and Environmental Microbiology, 63(10), 3933-3940. https://doi.org/10.1128/AEM.63.10.3933-3940.1997

Noda, H., Munderloh, U. G., & Kurtti, T. J. (1997). Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Applied and Environmental Microbiology, 63(10), 3926-3932. https://doi.org/10.1128/AEM.63.10.3926-3932.1997

Nováková, E., Hypša, V., & Moran, N. A. (2009). Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. BMC Microbiology, 9(1), 143. https://doi.org/10.1186/1471-2180-9-143

oksanOteo, J. A., Portillo, A., Portero, F., Zavala-Castro, J., Venzal, J. M., & Labruna, M. B. (2014). ’Candidatus Rickettsia asemboensis’ and Wolbachia spp. in Ctenocephalides felis and Pulex irritans fleas removed from dogs in Ecuador. Parasites & Vectors, 7(1), 455. https://doi.org/10.1186/s13071-014-0455-0

Parada, A. E., Needham, D. M., & Fuhrman, J. A. (2016). Every base matters: Assessing small subunit rRNA primers for marine microbiomes with mock communities, time series and global field samples. Environmental Microbiology, 18(5), 1403-1414. https://doi.org/10.1111/1462-2920.13023

Perotti, M. A., Kirkness, E. F., Reed, D. L., Braig, H. R., Bourtzis, K., & Miller, T. A. (2008). Endosymbionts of lice. In T. A. Miller (Ed.), Insect symbiosis (Vol. 3, pp. 205-220). CRC Press.

Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., & Glöckner, F. O. (2013). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41(D1), D590-D596. https://doi.org/10.1093/nar/gks1219

Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901-904. https://doi.org/10.1093/sysbio/syy032

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 Biology and Evolution, 9(11), 2946-2957. https://doi.org/10.1093/gbe/evx217

Rodríguez-Ruano, S. M., Juhaňáková, E., Vávra, J., & Nováková, E. (2020). Methodological insight into mosquito microbiome studies. Frontiers in Cellular and Infection Microbiology, 10, 86. https://doi.org/10.3389/fcimb.2020.00086

Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., & Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539-542. https://doi.org/10.1093/sysbio/sys029

Sauer, C., Stackebrandt, E., Gadau, J., Hölldobler, B., & Gross, R. (2000). Systematic relationships and cospeciation of bacterial endosymbionts and their carpenter ant host species: Proposal of the new taxon Candidatus Blochmannia gen. nov. International Journal of Systematic and Evolutionary Microbiology, 50(5), 1877-1886. https://doi.org/10.1099/00207713-50-5-1877

Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: An open-source platform for biological-image analysis. Nature Methods, 9(7), 676-682. https://doi.org/10.1038/nmeth.2019

Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671-675. https://doi.org/10.1038/nmeth.2089

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212. https://doi.org/10.1093/bioinformatics/btv351

Šochová, E., Husník, F., Nováková, E., Halajian, A., & Hypša, V. (2017). Arsenophonus and Sodalis replacements shape evolution of symbiosis in louse flies. PeerJ, 5, e4099. https://doi.org/10.7717/peerj.4099

Syberg-Olsen, M., Garber, A., Keeling, P., McCutcheon, J., & Husník, F. (2020). Pseudofinder, GitHub repository. Retrieved from https://github.com/filip-husnik/pseudofinder/

Vaser, R., Sović, I., Nagarajan, N., & Šikić, M. (2017). Fast and accurate de novo genome assembly from long uncorrected reads. Genome Research, 27(5), 737-746. https://doi.org/10.1101/gr.214270.116

Walters, W., Hyde, E. R., Berg-Lyons, D., Ackermann, G., Humphrey, G., Parada, A., Gilbert, J. A., Jansson, J. K., Caporaso, J. G., Fuhrman, J. A., Apprill, A., & Knight, R. (2016). Improved bacterial 16S rRNA gene (V4 and V4-5) and fungal internal transcribed spacer marker gene primers for microbial community surveys. mSystems, 1(1), e00009-15. https://doi.org/10.1128/mSystems.00009-15

Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 73(16), 5261-5267. https://doi.org/10.1128/AEM.00062-07

Waterworth, S. C., Flórez, L. V., Rees, E. R., Hertweck, C., Kaltenpoth, M., & Kwan, J. C. (2020). Horizontal gene transfer to a defensive symbiont with a reduced genome in a multipartite beetle microbiome. MBio, 11(1), e02430-19. https://doi.org/10.1128/mBio.02430-19

Yilmaz, L. S., Parnerkar, S., & Noguera, D. R. (2011). mathFISH, a web tool that uses thermodynamics-based mathematical models for in silico evaluation of oligonucleotide probes for fluorescence in situ hybridization. Applied and Environmental Microbiology, 77(3), 1118-1122. https://doi.org/10.1128/AEM.01733-10

Yun, J.-H., Roh, S. W., Whon, T. W., Jung, M.-J., Kim, M.-S., Park, D.-S., Yoon, C., Nam, Y.-D., Kim, Y.-J., Choi, J.-H., Kim, J.-Y., Shin, N.-R., Kim, S.-H., Lee, W.-J., & Bae, J.-W. (2014). Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Applied and Environmental Microbiology, 80(17), 5254-5264. https://doi.org/10.1128/AEM.01226-14

Fur microbiome as a putative source of symbiotic bacteria in sucking lice

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

Microbiomes of Blood-Feeding Triatomines in the Context of Their Predatory Relatives and the Environment

Supergroup F Wolbachia with extremely reduced genome: transition to obligate insect symbionts

Lightella neohaematopini: A new lineage of highly reduced endosymbionts coevolving with chipmunk lice of the genus Neohaematopinus

Zobrazit více v PubMed

Dryad
10.5061/dryad.76hdr7ssn, 10.5061/dryad.j9kd51c9v