'Candidatus Sarmatiella mevalonica' endosymbiont of the ciliate Paramecium provides insights on evolutionary plasticity among Rickettsiales.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
03 2021
03 2021
Historique:
revised:
07
01
2021
received:
28
10
2020
accepted:
08
01
2021
pubmed:
21
1
2021
medline:
16
10
2021
entrez:
20
1
2021
Statut:
ppublish
Résumé
Members of the bacterial order Rickettsiales are obligatorily associated with a wide range of eukaryotic hosts. Their evolutionary trajectories, in particular concerning the origin of shared or differential traits among distant sub-lineages, are still poorly understood. Here, we characterized a novel Rickettsiales bacterium associated with the ciliate Paramecium tredecaurelia and phylogenetically related to the Rickettsia genus. Its genome encodes significant lineage-specific features, chiefly the mevalonate pathway gene repertoire, involved in isoprenoid precursor biosynthesis. Not only this pathway has never been described in Rickettsiales, it also is very rare among bacteria, though typical in eukaryotes, thus likely representing a horizontally acquired trait. The presence of these genes could enable an efficient exploitation of host-derived intermediates for isoprenoid synthesis. Moreover, we hypothesize the reversed reactions could have replaced canonical pathways for producing acetyl-CoA, essential for phospholipid biosynthesis. Additionally, we detected phylogenetically unrelated mevalonate pathway genes in metagenome-derived Rickettsiales sequences, likely indicating evolutionary convergent effects of independent horizontal gene transfer events. Accordingly, convergence, involving both gene acquisitions and losses, is highlighted as a relevant evolutionary phenomenon in Rickettsiales, possibly favoured by plasticity and comparable lifestyles, representing a potentially hidden origin of other more nuanced similarities among sub-lineages.
Identifiants
pubmed: 33470507
doi: 10.1111/1462-2920.15396
doi:
Substances chimiques
RNA, Ribosomal, 16S
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1684-1701Informations de copyright
© 2021 Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Ahyong, V., Berdan, C.A., Burke, T.P., Nomura, D.K., and Welch, M.D. (2019) A metabolic dependency for host isoprenoids in the obligate intracellular pathogen Rickettsia parkeri underlies a sensitivity to the statin class of host-targeted therapeutics. MSphere 4: e00536-e00519.
Andersson, S.G.E., Zomorodipour, A., Andersson, J.O., Sicheritz-Pontén, T., Alsmark, U.C.M., Podowski, R.M., et al. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396: 133-143.
Almagro Armenteros, J.J., Tsirigos, K.D., Sønderby, C.K., Nordahl Petersen, T., Winther, O., et al. (2019) SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 37: 420-423.
Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R., and Stahl, D.A. (1990) Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925.
Arndt, D., Grant, J.R., Marcu, A., Sajed, T., Pon, A., Liang, Y., and Wishart, D.S. (2016) PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res 44: W16-W21.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., et al. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19: 455-477.
Beckmann, J.F., Bonneau, M., Chen, H., Hochstrasser, M., Poinsot, D., Merçot, H., et al. (2019) The toxin-antidote model of cytoplasmic incompatibility: genetics and evolutionary implications. Trends Genet 35: 175-185.
Bella, C., Koehler, L., Grosser, K., Berendonk, T.U., Petroni, G., and Schrallhammer, M. (2016) Fitness impact of obligate intranuclear bacterial symbionts depends on host growth phase. Front Microbiol 7: 2084 -.
Blocker, A., Komoriya, K., and Aizawa, S.I. (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci 100: 3027-3030.
Borisov, V.B., Gennis, R.B., Hemp, J., and Verkhovsky, M.I. (2011) The cytochrome bd respiratory oxygen reductases. Biochimica et Biophysica Acta (BBA) - Bioenergetics 1807: 1398-1413.
Braig, H.R., Guzman, H., Tesh, R.B., and O'Neill, S.L. (1994) Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367: 453-455.
Castelli, M., Sassera, D., and Petroni, G. (2016) Biodiversity of “non-model” Rickettsiales and their association with aquatic organisms. In Rickettsiales-Biology, Molecular Biology, Epidemiology, and Vaccine Development, Thomas, S. (ed). Cham, Switzerland: Springer International Publishing, pp. 59-91.
Castelli, M., Sabaneyeva, E., Lanzoni, O., Lebedeva, N., Floriano, A.M., Gaiarsa, S., et al. (2019a) Deianiraea, an extracellular bacterium associated with the ciliate Paramecium, suggests an alternative scenario for the evolution of Rickettsiales. ISME J 13: 2280-2294.
Castelli, M., Serra, V., Senra, M.V.X., Basuri, C.K., Soares, C.A.G., Fokin, S.I., et al. (2019b) The hidden world of Rickettsiales symbionts: “Candidatus Spectririckettsia obscura,” a novel bacterium found in Brazilian and Indian Paramecium caudatum. Microb Ecol 77: 748-758.
Chaumeil, P.A., Mussig, A.J., Hugenholtz, P., and Parks, D.H. (2020) GTDB-Tk: a toolkit to classify genomes with the genome taxonomy database. Bioinformatics 36: 1925-1927.
Chee, J.Y., Yoga, S.S., Lau, N.S., Ling, S.C., Abed, R.M.M., and Sudesh, K. (2010) Bacterially produced polyhydroxyalkanoate (PHA): converting renewable resources into bioplastic. In Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, Méndez-Vilas, A. (ed). Badajoz, Spain: Formatex Research Center, pp. 1395-1404.
Cole, J.R., Wang, Q., Fish, J.A., Chai, B., McGarrell, D.M., Sun, Y., et al. (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42: D633-D642.
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772.
Driscoll, T.P., Verhoeve, V.I., Guillotte, M.L., Lehman, S.S., Rennoll, S.A., Beier-Sexton, M., et al. (2017) Wholly Rickettsia! Reconstructed metabolic profile of the quintessential bacterial parasite of eukaryotic cells. MBio 8: e00859-e00817.
Duncan, A.B., Fellous, S., Accot, R., Alart, M., Sobandi, K.C., Cosiaux, A., and Kaltz, O. (2010) Parasite-mediated protection against osmotic stress for Paramecium caudatum infected by Holospora undulata is host genotype specific. FEMS Microbiol Ecol 74: 353-360.
Dunning Hotopp, J.C., Lin, M., Madupu, R., Crabtree, J., Angiuoli, S.V., Eisen, J., et al. (2006) Comparative genomics of emerging human ehrlichiosis agents. PLoS Genet 2: e21.
Duplouy, A., Iturbe-Ormaetxe, I., Beatson, S.A., Szubert, J.M., Brownlie, J.C., McMeniman, C.J., et al. (2013) Draft genome sequence of the male-killing Wolbachia strain wBol1 reveals recent horizontal gene transfers from diverse sources. BMC Genomics 14: 20.
Duron, O., Doublet, P., Vavre, F., and Bouchon, D. (2018) The importance of revisiting Legionellales diversity. Trends Parasitol 34: 1027-1037.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
El Karkouri, K., Pontarotti, P., Raoult, D., and Fournier, P.E. (2016) Origin and evolution of rickettsial plasmids. PLoS One 11: e0147492.
Epis, S., Sassera, D., Beninati, T., Lo, N., Beati, L., Piesman, J., et al. (2018) Midichloria mitochondrii is widespread in hard ticks (Ixodidae) and resides in the mitochondria of phylogenetically diverse species. Parasitology 135: 485-494.
Floriano, A.M., Castelli, M., Krenek, S., Berendonk, T.U., Bazzocchi, C., Petroni, G., and Sassera, D. (2018) The genome sequence of “Candidatus Fokinia solitaria”: insights on reductive evolution in Rickettsiales. Genome Biol Evol 10: 1120-1126.
Görtz, H.D., and Fokin, S.I. (2009) Diversity of endosymbiotic bacteria in Paramecium. In Endosymbionts in Paramecium, Fujishima, M. (ed). Berlin-Heidelberg, Germany: Springer, pp. 131-160.
Galperin, M.Y., Makarova, K.S., Wolf, Y.I., and Koonin, E.V. (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Res 43: D261-D269.
George, E.E., Husnik, F., Tashyreva, D., Prokopchuk, G., Horák, A., Kwong, W.K., et al. (2020) Highly reduced genomes of protist endosymbionts show evolutionary convergence. Curr Biol 30: 925-933.e3.
Gillespie, J.J., Ammerman, N.C., Dreher-Lesnick, S.M., Rahman, M.S., Worley, M.J., Setubal, J.C., et al. (2009) An anomalous type IV secretion system in Rickettsia is evolutionarily conserved. PLoS ONE 4: e4833.
Gillespie, J.J., Joardar, V., Williams, K.P., Driscoll, T., Hostetler, J.B., Nordberg, E., et al. (2012) A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. J Bacteriol 194: 376-394.
Gillespie, J.J., Kaur, S.J., Rahman, M.S., Rennoll-Bankert, K., Sears, K.T., Beier-Sexton, M., and Azad, A.F. (2015) Secretome of obligate intracellular Rickettsia. FEMS Microbiol Rev 39: 47-80.
Gillespie, J.J., Phan, I.Q., Driscoll, T.P., Guillotte, M.L., Lehman, S.S., Rennoll-Bankert, K.E., et al. (2016) The Rickettsia type IV secretion system: unrealized complexity mired by gene family expansion. Pathogens Dis 74: ftw058.
Gomez-Valero, L., Rusniok, C., Jarraud, S., Vacherie, B., Rouy, Z., Barbe, V., et al. (2011) Extensive recombination events and horizontal gene transfer shaped the Legionella pneumophila genomes. BMC Genomics 12: 536.
Gottlieb, Y., Lalzar, I., and Klasson, L. (2015) Distinctive genome reduction rates revealed by genomic analyses of two Coxiella-like endosymbionts in ticks. Genome Biol Evol 7: 1779-1796.
Greuter, D., Loy, A., Horn, M., and Rattei, T. (2016) probeBase--an online resource for rRNA-targeted oligonucleotide probes and primers: new features. Nucleic Acids Res 44: D586-D589.
Gruber-Vodicka, H.R., Leisch, N., Kleiner, M., Hinzke, T., Liebeke, M., McFall-Ngai, M., et al. (2019) Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2. Nat Microbiol 4: 1465-1474.
Horn, M., Collingro, A., Schmitz-Esser, S., Beier, C.L., Purkhold, U., Fartmann, B., et al. (2004) Illuminating the evolutionary history of Chlamydiae. Science 304: 728-730.
Hoshino, Y., and Gaucher, E.A. (2018) On the origin of isoprenoid biosynthesis. Mol Biol Evol 35: 2185-2197.
Kanehisa, M., Sato, Y., Furumichi, M., Morishima, K., and Tanabe, M. (2019) New approach for understanding genome variations in KEGG. Nucl Acids Res 47: D590-D595.
Kang, Y.J., Diao, X.N., Zhao, G.Y., Chen, M.H., Xiong, Y., Shi, M., et al. (2014) Extensive diversity of Rickettsiales bacteria in two species of ticks from China and the evolution of the Rickettsiales. BMC Evol Biol 14: 167.
Karp, P.D., Billington, R., Caspi, R., Fulcher, C.A., Latendresse, M., Kothari, A., et al. (2019) The BioCyc collection of microbial genomes and metabolic pathways. Brief Bioinformatics 20: 1085-1093.
Kent, B.N., and Bordenstein, S.R. (2010) Phage WO of Wolbachia: lambda of the endosymbiont world. Trends Microbiol 18: 173-181.
Kikuchi, Y., and Fukatsu, T. (2015) Rickettsia infection in natural leech populations. Microb Ecol 49: 265-271.
Klasson, L., Westberg, J., Sapountzis, P., Näslund, K., Lutnaes, Y., Darby, A.C., et al. (2009) The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc Natl Acad Sci 106: 5725-5730.
Klinges, J.C., Rosales, S.M., McMinds, R., Shaver, E.C., Shantz, A.A., Peters, E.C., et al. (2019) Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov. ISME J 13: 2938-2953.
Kumar, S., Jones, M., Koutsovoulos, G., Clarke, M., and Blaxter, M. (2013) Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots. Front Genet 4: 237.
Langmead, B., and Salzberg, S.L. (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357-359.
Lanzoni, O., Fokin, S.I., Lebedeva, N., Migunova, A., Petroni, G., and Potekhin, A. (2016) Rare freshwater ciliate Paramecium chlolarelligerum Kahl, 1935 and its macronuclear symbiotic bacterium “Candidatus Holospora parva”. PLoS One 11: e0167928.
Lanzoni, O., Sabaneyeva, E., Modeo, L., Castelli, M., Lebedeva, N., Verni, F., et al. (2019) Diversity and environmental distribution of the cosmopolitan endosymbiont “Candidatus Megaira”. Sci Rep 9: 1179.
Lin, H., Lou, B., Glynn, J.M., Doddapaneni, H., Civerolo, E.L., Chen, C., et al. (2011) The complete genome sequence of 'Candidatus Liberibacter solanacearum', the bacterium associated with potato zebra chip disease. PLoS One 6: e19135.
Lombard, J., and Moreira, D. (2011) Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol Biol Evol 28: 87-99.
Manz, W., Amann, R.I., Ludwig, W., Wagner, M., and Schleifer, K.H. (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of Proteobacteria: problems and solutions. Syst Appl Microbiol 15: 593-600.
Martijn, J., Schulz, F., Zaremba-Niedzwiedzka, K., Viklund, J., Stepanauskas, R., Andersson, S.G.E., et al. (2015) Single-cell genomics of a rare environmental alphaproteobacterium provides unique insights into Rickettsiaceae evolution. ISME J 9: 2373-2385.
Matic, I., Rayssiguier, C., and Radman, M. (1995) Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80: 507-515.
Matsuura, Y., Kikuchi, Y., Meng, X.Y., Koga, R., and Fukatsu, T. (2012) Novel clade of alphaproteobacterial endosymbionts associated with stinkbugs and other arthropods. Appl Environ Microbiol 78: 4149-4156.
McCutcheon, J.P., and Moran, N. (2012) Extreme genome reduction in symbiotic bacteria. Nat Rev Biotechnol 10: 13-26.
Mediannikov, O., Nguyen, T.T., Bell-Sakyi, L., Padmanabhan, R., Fournier, P.E., and Raoult, D. (2014) High quality draft genome sequence and description of Occidentia massiliensis gen. nov., sp. nov., a new member of the family Rickettsiaceae. Stand Genomic Sci 9: 9.
Midha, S., Rigden, D.J., Siozios, S., Hurst, G.D.D., and Jackson, A.P. (2020) The Paracaedibacter-like endosymbiont of Bodo saltans (Kinetoplastida) uses multiple putative toxin-antitoxin systems to maintain its host association. BioRxiv. https://doi.org/10.1101/2020.07.24.21713
Min, C.K., Yang, J.S., Kim, S., Choi, M.S., Kim, I.S., and Cho, N.H. (2008) Genome-based construction of the metabolic pathways of Orientia tsutsugamushi and comparative analysis within the Rickettsiales order. Comp Funct Genomics 2008: 623145.
Modeo, L., Salvetti, A., Rossi, L., Castelli, M., Szokoli, F., Krenek, S., et al. (2020) “Candidatus Trichorickettsia mobilis”, a Rickettsiales bacterium, can be transiently transferred from the unicellular eukaryote Paramecium to the planarian Dugesia japonica. PeerJ 8: e8977.
Muñoz-Gómez, S., Hess, S., Burger, G., Lang, B.F., Susko, E., Slamovits, C.H., et al. (2019) An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. eLife 8: e42535.
Murray, R.G., and Stackebrandt, E. (1995) Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol 45: 186-187.
Nakamura, T., Yamada, K.D., Tomii, K., and Katoh, K. (2018) Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34: 2490-2492.
Nikoh, N., Hosokawa, T., Moriyama, M., Oshima, K., Hattori, M., and Fukatsu, T. (2014) Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci 111: 10257-10262.
Ogata, H., La Scola, B., Audic, S., Renesto, P., Blanc, G., Robert, C., et al. (2006) Genome sequence of Rickettsia bellii illuminates the role of amoebae in gene exchanges between intracellular pathogens. PLoS Genet 2: e76.
Olivieri, E., Epis, S., Castelli, M., Varotto Boccazzi, I., Romeo, C., Desirò, A., et al. (2019) Tissue tropism and metabolic pathways of Midichloria mitochondrii suggest tissue-specific functions in the symbiosis with Ixodes ricinus. Ticks Tick Borne Dis 10: 1070-1077.
Oren, A., Garrity, G.M., Parker, C.T., Chuvochina, M., and Trujillo, M.E. (2020) Lists of names of prokaryotic Candidatus taxa. Int J Syst Evol Microbiol 70: 3956-4042.
Parks, D.H., Chuvochina, M., Waite, D.W., Rinke, C., Skarshewski, A., Chaumeil, P.A., and Hugenholtz, P. (2018) A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36: 996-1004.
Perlman, S.J., Hunter, M.S., and Zchori-Fein, E. (2006) The emerging diversity of Rickettsia. Proc R Soc B 273: 2097-2106.
Pilgrim, J., Ander, M., Garros, C., Baylis, M., Hurst, G.D.D., and Siozios, S. (2017) Torix group Rickettsia are widespread in Culicoides biting midges (Diptera: Ceratopogonidae), reach high frequency and carry unique genomic features. Environ Microbiol 19: 4238-4255.
Pirritano, M., Zaburannyi, N., Grosser, K., Gasparoni, G., Müller, R., Simon, M., and Schrallhammer, M. (2020) Dual-Seq reveals genome and transcriptome of Caedibacter taeniospiralis, obligate endosymbiont of Paramecium. Sci Rep 10: 9727.
Przyboś, E., Tarcz, S., Surmacz, M., Sawka, N., and Fokin, S.I. (2013) Paramecium tredecaurelia: a unique non-polymorphic species of the P. aurelia spp. complex (Oligohymenophorea, Ciliophora). Acta Protozool 52: 257-266.
Puigbo, P., Bravo, I.G., and Garcia-Vallve, S. (2008) CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 3: 38.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., et al. (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl Acids Res 41: D590-D596.
Rikihisa, Y. (2010) Anaplasma phagocytophilum and Ehrlichia chaffeensis: subversive manipulators of host cells. Nat Rev Microbiol 8: 328-339.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., et al. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61: 539-542.
Sabaneyeva, E., Castelli, M., Szokoli, F., Benken, K., Lebedeva, N., Salvetti, A., et al. (2018) Host and symbiont intraspecific variability: the case of Paramecium calkinsi and “Candidatus Trichorickettsia mobilis”. Eur J Protistol 62: 79-94.
Sassera, D., Lo, N., Epis, S., D'Auria, G., Montagna, M., Comandatore, F., et al. (2011) Phylogenomic evidence for the presence of a flagellum and cbb3 oxidase in the free-living mitochondrial ancestor. Mol Biol Evol 28: 3285-3296.
Schrallhammer, M., and Potekhin, A. (2020) Epidemiology of nucleus-dwelling Holospora: infection, transmission, adaptation, and interaction with Paramecium. In Symbiosis: Cellular, Molecular, Medical and Evolutionary Aspects, Vol. 69, Kloc, M. (ed) . Cham: Springer, pp. 105-135.Results and Problems in Cell Differentiation
Schu, M.G., and Schrallhammer, M. (2018) Cultivation conditions can cause a shift from mutualistic to parasitic behavior in the symbiosis between Paramecium and its bacterial symbiont Caedibacter taeniospiralis. Curr Microbiol 75: 1099-1102.
Schulz, F., Martijn, J., Wascher, F., Lagkouvardos, I., Kostanjšek, R., Ettema, T.J.G., and Horn, M. (2016) A Rickettsiales symbiont of amoebae with ancient features. Environ Microbiol 18: 2326-2342.
Seemann, T. (2013) barrnap 0.5 : rapid ribosomal RNA prediction. URL: http://www.vicbioinformatics.com/
Seemann, T. (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068-2069.
Serra, V., Gammuto, L., Nitla, N., Castelli, M., Lanzoni, O., Sassera, D., et al. (2020) Morphology, ultrastructure, genomics, and phylogeny of Euplotes vanleeuwenhoeki sp. nov. and its ultra-reduced endosymbiont “Candidatus Pinguicoccus supinus” sp. nov. Sci Rep 10: 20311.
Siddiqi, M.A., and Rodwell, V.W. (1967) Bacterial metabolism of mevalonic acid. J Bacteriol 93: 207-214.
Siguier, P., Perochon, J., Lestrade, L., Mahillon, J., and Chandler, M. (2006) ISfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res 34: D32-D36.
Silverman, D.J., Wisseman, C.L., Jr., Waddell, A.D., and Jones, M. (1978) External layers of Rickettsia prowazekii and Rickettsia rickettsii: occurrence of a slime layer. Infect Immun 22: 233-246.
Simão, F.A., Waterhouse, R.M., Ioannidis, P., Kriventseva, E.V., and Zdobnov, E.M. (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31: 3210-3212.
Stamatakis, A. (2015) Using RAxML to infer phylogenies. Curr Protoc Bioinform 51: 6.14.1-6.14.14.
Szokoli, F., Castelli, M., Sabaneyeva, E., Schrallhammer, M., Krenek, S., Doak, T.G., et al. (2016a) Disentangling the taxonomy of Rickettsiales and description of two novel symbionts (“Candidatus Bealeia paramacronuclearis” and “Candidatus Fokinia cryptica”) sharing the cytoplasm of the ciliate protist Paramecium biaurelia. Appl Environ Microbiol 82: 7236-7247.
Szokoli, F., Sabaneyeva, E., Castelli, M., Krenek, S., Schrallhammer, M., Soares, C.A.G., et al. (2016b) “Candidatus Fokinia solitaria”, a novel “stand-alone” symbiotic lineage of Midichloriaceae (Rickettsiales). PLoS One 11: e0145743.
Takatsuji, H., Nishino, T., Miki, I., and Katsuki, H. (1983) Studies on isoprenoid biosynthesis with bacterial intact cells. Biochem Biophys Res Commun 110: 187-193.
Taylor, M.J., Bandi, C., and Hoerauf, A. (2005) Wolbachia endosymbionts of filarial nematodes. Adv Parasitol 60: 245-284.
Talavera, G., and Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564-577.
Vannini, C., Petroni, G., Verni, F., and Rosati, G. (2004) A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Microb Ecol 49: 434-442.
Vannini, C., Boscaro, V., Ferrantini, F., Benken, K.A., Mironov, T.I., Schweikert, M., et al. (2014) Flagellar movement in two bacteria of the family Rickettsiaceae: a re-evaluation of motility in an evolutionary perspective. PLoS One 9: e8771.
Walker, D.H., and Ismail, N. (2008) Emerging and re-emerging rickettsioses: endothelial cell infection and early disease events. Nat Rev Microbiol 6: 375-386.
Wang, Z., and Wu, M. (2017) Comparative genomic analysis of Acanthamoeba endosymbionts highlights the role of amoebae as a "melting pot" shaping the Rickettsiales evolution. Genome Biol Evol 9: 3214-3224.
Wang, H.L., Lei, T., Wang, X.W., Maruthi, M.N., Zhu, D.T., Cameron, S.L., et al. (2020) A newly recorded Rickettsia of the Torix group is a recent intruder and an endosymbiont in the whitefly Bemisia tabaci. Environ Microbiol 22: 1207-1221.
Weinert, L.A., Werren, J.H., Aebi, A., Stone, G.N., and Jiggins, F.M. (2009) Evolution and diversity of Rickettsia bacteria. BMC Biol 7: 6.
Westram, R., Bader, K., Prüsse, E., Kumar, Y., Meier, H., Glöckner, F.O., and Ludwig, W. (2011) ARB: a software environment for sequence data. In Handbook of Molecular Microbial Ecology I: Metagenomics and Complementary Approaches, de Bruijn, F.J. (ed). Hoboken, NJ: John Wiley & Sons, pp. 399-406.
Yan, Y., Jiang, L., Aufderheide, K.J., Wright, G.A., Terekhov, A., Costa, L., et al. (2014) A microfluidic-enabled mechanical microcompressor for the immobilization of live single- and multi-cellular specimens. Microsc Microanal 20: 141-151.
Yang, A., Narechania, A., and Kim, E. (2016) Rickettsial endosymbiont in the “early-diverging” streptophyte green alga Mesostigma viride. J Phycol 52: 219-229.
Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F.O., Ludwig, W., & Schleifer, K.H. (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12: 635-645.
Yurchenko, T., Ševčíková, T., Přibyl, P., El Karkouri, K., Klimeš, V., Amaral, R., et al. (2018) A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria. ISME J 12: 2163-2175.