Novel evolutionary insights on the interactions of the Holosporales (Alphaproteobacteria) with eukaryotic hosts from comparative genomics.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
03 Jan 2024
03 Jan 2024
Historique:
received:
12
06
2023
accepted:
11
12
2023
medline:
4
1
2024
pubmed:
4
1
2024
entrez:
4
1
2024
Statut:
aheadofprint
Résumé
Holosporales are an alphaproteobacterial order engaging in obligate and complex associations with eukaryotes, in particular protists. The functional and evolutionary features of those interactions are still largely undisclosed. Here, we sequenced the genomes of two members of the species Bealeia paramacronuclearis (Holosporales, Holosporaceae) intracellularly associated with the ciliate protist Paramecium, which resulted in high correspondence. Consistent with the short-branched early-divergent phylogenetic position, Bealeia presents a larger functional repertoire than other Holosporaceae, comparable to those of other Holosporales families, particularly for energy metabolism and motility. Our analyses indicate that different Holosporales likely experienced at least partly autonomous genome reduction and adaptation to host interactions, for example regarding dependence on host biotin driven by multiple independent horizontal acquisitions of transporters. Among Alphaproteobacteria, this is reminiscent of the convergently evolved Rickettsiales, which however appear more diverse, possibly due to a probably more ancient origin. We identified in Bealeia and other Holosporales the plasmid-encoded putative genetic determinants of R-bodies, which may be involved in a killer trait towards symbiont-free hosts. While it is not clear whether these genes are ancestral or recently horizontally acquired, an intriguing and peculiar role of R-bodies is suggested in the evolution of the interactions of multiple Holosporales with their hosts.
Identifiants
pubmed: 38173299
doi: 10.1111/1462-2920.16562
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : H2020 Marie Skłodowska-Curie Actions
ID : RISE 872767
Organisme : Università di Pisa
ID : PRA_ 2018_63
Informations de copyright
© 2024 The Authors. Environmental Microbiology published by Applied Microbiology International and John Wiley & Sons Ltd.
Références
Abby, S.S. & Rocha, E.P.C. (2012) The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genetics, 8, e1002983.
Aussel, L., Pierrel, F., Loiseau, L., Lombard, M., Fontecave, M. & Barras, F. (2014) Biosynthesis and physiology of coenzyme Q in bacteria. Biochimica et Biophysica Acta, 1837, 1004-1011.
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. Journal of Computational Biology, 19, 455-477.
Beliavskaia, A.Y., Predeus, A.V., Garushyants, S.K., Logacheva, M.D., Gong, J., Zou, S. et al. (2020) New Intranuclear symbiotic bacteria from macronucleus of paramecium putrinum-’Candidatus Gortzia Yakutica’. Diversity, 12, 198.
Bennett, G.M., McCutcheon, J.P., MacDonald, B.R., Romanovicz, D. & Moran, N.A. (2014) Differential genome evolution between companion symbionts in an insect-bacterial symbiosis. MBio, 5, e01697.
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, 112, 10169-10176.
Benz, R. (2016) Channel formation by RTX-toxins of pathogenic bacteria: basis of their biological activity. Biochimica et Biophysica Acta, 1858, 526-537.
Betts-Hampikian, H.J. & Fields, K.A. (2010) The chlamydial type III secretion mechanism: revealing cracks in a tough nut. Frontiers in Microbiology, 1, 114.
Birtles, R.J., Rowbotham, T.J., Michel, R., Pitcher, D.G., Lascola, B., Alexiou-Daniel, S. et al. (2000) ‘Candidatus Odyssella thessalonicensis’ gen. Nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. International Journal of Systematic and Evolutionary Microbiology, 50(1), 63-72.
Borisov, V.B., Gennis, R.B., Hemp, J. & Verkhovsky, M.I. (2011) The cytochrome bd respiratory oxygen reductases. Biochimica et Biophysica Acta, 1807, 1398-1413.
Borowiec, M.L. (2016) AMAS: a fast tool for alignment manipulation and computing of summary statistics. PeerJ, 4, e1660.
Boscaro, V., Husnik, F., Vannini, C. & Keeling, P.J. (2019) Symbionts of the ciliate Euplotes: diversity, patterns and potential as models for bacteria-eukaryote endosymbioses. Proceedings of the Biological Sciences, 286, 20190693.
Buysse, M., Floriano, A.M., Gottlieb, Y., Nardi, T., Comandatore, F., Olivieri, E. et al. (2021) A dual endosymbiosis supports nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum. eLife, 10, e72747.
Cantalapiedra, C.P., Hernández-Plaza, A., Letunic, I., Bork, P. & Huerta-Cepas, J. (2021) eggNOG-mapper v2: functional annotation, Orthology assignments, and domain prediction at the metagenomic scale. Molecular Biology and Evolution, 38, 5825-5829.
Carver, T., Thomson, N., Bleasby, A., Berriman, M. & Parkhill, J. (2009) DNAPlotter: circular and linear interactive genome visualization. Bioinformatics, 25, 119-120.
Castelli, M., Lanzoni, O., Giovannini, M., Lebedeva, N., Gammuto, L., Sassera, D. et al. (2022) Candidatus Gromoviella agglomerates, a novel intracellular Holosporaceae parasite of the ciliate paramecium showing marked genome reduction. Environmental Microbiology Reports, 14, 34-49.
Castelli, M., Lanzoni, O., Nardi, T., Lometto, S., Modeo, L., Potekhin, A. et al. (2021) ‘Candidatus Sarmatiella mevalonica’ endosymbiont of the ciliate paramecium provides insights on evolutionary plasticity among Rickettsiales. Environmental Microbiology, 23, 1684-1701.
Castelli, M., Nardi, T., Gammuto, L., Bellinzona, G., Sabaneyeva, E., Potekhin, A. et al. (2022) Host association and intracellularity evolved multiple times independently in the Rickettsiales. bioRxiv. 511287. https://doi.org/10.1101/2022.10.13.511287
Castelli, M., Sabaneyeva, E., Lanzoni, O., Lebedeva, N., Floriano, A.M., Gaiarsa, S. et al. (2019) Deianiraea, an extracellular bacterium associated with the ciliate paramecium, suggests an alternative scenario for the evolution of Rickettsiales. The ISME Journal, 13, 2280-2294.
Castelli, M., Sassera, D. & Petroni, G. (2016) Biodiversity of ‘non-model’ Rickettsiales and their association with aquatic organisms. In: Rickettsiales: Biology, molecular biology, epidemiology, and vaccine development, Switzerland: Springer, Cham, pp. 59-91.
Chauhan, D. & Shames, S.R. (2021) Pathogenicity and virulence of legionella: intracellular replication and host response. Virulence, 12, 1122-1144.
Collingro, A., Köstlbacher, S. & Horn, M. (2020) Chlamydiae in the environment. Trends in Microbiology, 28, 877-888.
Collingro, A., Köstlbacher, S., Mussmann, M., Stepanauskas, R., Hallam, S.J. & Horn, M. (2017) Unexpected genomic features in widespread intracellular bacteria: evidence for motility of marine chlamydiae. The ISME Journal, 11, 2334-2344.
Criscuolo, A. & Gribaldo, S. (2010) BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evolutionary Biology, 10, 210.
Csűrös, M. (2010) Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics, 26, 1910-1912.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics, 27, 1164-1165.
Dharamshi, J.E., Tamarit, D., Eme, L., Stairs, C.W., Martijn, J., Homa, F. et al. (2020) Marine sediments illuminate Chlamydiae diversity and evolution. Current Biology: CB, 30, 1032-1048.e7.
Dittmer, J., Bredon, M., Moumen, B., Raimond, M., Grève, P. & Bouchon, D. (2023) The terrestrial isopod symbiont ‘Candidatus Hepatincola porcellionum’ is a potential nutrient scavenger related to Holosporales symbionts of protists. ISME Communications, 3, 18.
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(5), e00859-17.
Duron, O., Doublet, P., Vavre, F. & Bouchon, D. (2018) The importance of revisiting Legionellales diversity. Trends in Parasitology, 34, 1027-1037.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797.
Elwell, C., Mirrashidi, K. & Engel, J. (2016) Chlamydia cell biology and pathogenesis. Nature Reviews. Microbiology, 14, 385-400.
Emms, D.M. & Kelly, S. (2019) OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biology, 20, 238.
Ferla, M.P. & Patrick, W.M. (2014) Bacterial methionine biosynthesis. Microbiology, 160, 1571-1584.
Floriano, A.M., Batisti Biffignandi, G., Castelli, M., Olivieri, E., Clementi, E., Comandatore, F. et al. (2022) The origin and evolution of mitochondrial tropism in Midichloria bacteria. bioRxiv. https://doi.org/10.1101/2022.05.16.490919
Floriano, A.M., Castelli, M., Krenek, S., Berendonk, T.U., Bazzocchi, C., Petroni, G. et al. (2018) The genome sequence of ‘Candidatus Fokinia solitaria’: insights on reductive evolution in Rickettsiales. Genome Biology and Evolution, 10, 1120-1126.
Galperin, M.Y., Makarova, K.S., Wolf, Y.I. & Koonin, E.V. (2015) Expanded microbial genome coverage and improved protein family annotation in the COG database. Nucleic Acids Research, 43, D261-D269.
Garushyants, S.K., Beliavskaia, A.Y., Malko, D.B., Logacheva, M.D., Rautian, M.S. & Gelfand, M.S. (2018) Comparative genomic analysis of Holospora spp., Intranuclear symbionts of paramecia. Frontiers in Microbiology, 9, 738.
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. Current Biology, 30, 925-933.e3.
Georgiades, K., Madoui, M.-A., Le, P., Robert, C. & Raoult, D. (2011) Phylogenomic analysis of Odyssella thessalonicensis fortifies the common origin of Rickettsiales, Pelagibacter ubique and Reclimonas Americana mitochondrion. PLoS One, 6, e24857.
Gillespie, J.J., Brayton, K.A., Williams, K.P., Diaz, M.A.Q., Brown, W.C., Azad, A.F. et al. (2010) Phylogenomics reveals a diverse Rickettsiales type IV secretion system. Infection and Immunity, 78, 1809-1823.
Gillespie, J.J., Kaur, S.J., Rahman, M.S., Rennoll-Bankert, K., Sears, K.T., Beier-Sexton, M. et al. (2014) Secretome of obligate intracellular rickettsia. FEMS Microbiology Reviews, 39, 47-80.
Goris, J., Konstantinidis, K.T., Klappenbach, J.A., Coenye, T., Vandamme, P. & Tiedje, J.M. (2007) DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. International Journal of Systematic and Evolutionary Microbiology, 57, 81-91.
Guidetti, R., Vecchi, M., Ferrari, A., Newton, I.L.G., Cesari, M. & Rebecchi, L. (2020) Further insights in the Tardigrada microbiome: phylogenetic position and prevalence of infection of four new Alphaproteobacteria putative endosymbionts. Zoological Journal of the Linnean Society, 188, 925-937.
Hess, S., Suthaus, A. & Melkonian, M. (2016) ‘Candidatus Finniella’ (Rickettsiales, Alphaproteobacteria), novel endosymbionts of Viridiraptorid Amoeboflagellates (Cercozoa, Rhizaria). Applied and Environmental Microbiology, 82, 659-670.
Horn, M., Fritsche, T.R., Gautom, R.K., Schleifer, K.H. & Wagner, M. (1999) Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environmental Microbiology, 1, 357-367.
Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S.K., Cook, H. et al. (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309-D314.
Hugoson, E., Guliaev, A., Ammunét, T. & Guy, L. (2022) Host adaptation in Legionellales is 1.9 Ga, coincident with Eukaryogenesis. Molecular Biology and Evolution, 39, e037.
Husnik, F., Tashyreva, D., Boscaro, V., George, E.E., Lukeš, J. & Keeling, P.J. (2021) Bacterial and archaeal symbioses with protists. Current Biology, 31, R862-R877.
Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K.F., von Haeseler, A. & Jermiin, L.S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14, 587-589.
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, D457-D462.
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. Briefings in Bioinformatics, 20, 1085-1093.
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772-780.
Kobryn, K. & Chaconas, G. (2002) ResT, a telomere resolvase encoded by the Lyme disease spirochete. Molecular Cell, 9, 195-201.
Konecka, E. & Olszanowski, Z. (2019) Detection of a new bacterium of the family Holosporaceae (Alphaproteobacteria: Holosporales) associated with the oribatid mite Achipteria coleoptrata. Biologia (Bratisl), 74, 1517-1522.
Korotaev, A., Benken, K. & Sabaneyeva, E. (2020) ‘Candidatus Mystax nordicus’ aggregates with mitochondria of its host, the ciliate paramecium nephridiatum. Diversity, 12, 251.
Kroer, P., Kjeldsen, K.U., Nyengaard, J.R., Schramm, A. & Funch, P. (2016) A novel extracellular gut symbiont in the marine worm Priapulus caudatus (Priapulida) reveals an Alphaproteobacterial symbiont clade of the Ecdysozoa. Frontiers in Microbiology, 7, 539.
Kumar, S., Jones, M., Koutsovoulos, G., Clarke, M. & Blaxter, M. (2013) Blobology: exploring raw genome data for contaminants, symbionts and parasites using taxon-annotated GC-coverage plots. Frontiers in Genetics, 4, 237.
Langmead, B. & Salzberg, S.L. (2012) Fast gapped-read alignment with bowtie 2. Nature Methods, 9, 357-359.
Leyva, J.M., Martínez-Porchas, M., Vargas-Albores, F., Hernández-López, J. & Gollas-Galván, T. (2017) Análisis bioinformático del sistema flagelar de la alphaproteobacteria tipo rickettsia Candidatus Hepatobacter penaei. Revista de Biología Marina y Oceanografía, 52, 121-130.
Lin, M. & Rikihisa, Y. (2003) Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid a biosynthesis and incorporate cholesterol for their survival. Infection and Immunity, 71, 5324-5331.
Little, D.J., Li, G., Ing, C., DiFrancesco, B.R., Bamford, N.C., Robinson, H. et al. (2014) Modification and periplasmic translocation of the biofilm exopolysaccharide poly-β-1,6-N-acetyl-D-glucosamine. Proceedings of the National Academy of Sciences of the United States of America, 111, 11013-11018.
Major, P., Embley, T.M. & Williams, T.A. (2017) Phylogenetic diversity of NTT nucleotide transport proteins in free-living and parasitic bacteria and eukaryotes. Genome Biology and Evolution, 9, 480-487.
Marçais, G., Delcher, A.L., Phillippy, A.M., Coston, R., Salzberg, S.L. & Zimin, A. (2018) MUMmer4: A fast and versatile genome alignment system. PLoS Computational Biology, 14, e1005944.
McFall-Ngai, M., Hadfield, M.G., Bosch, T.C.G., Carey, H.V., Domazet-Lošo, T., Douglas, A.E. et al. (2013) Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences, 110, 3229-3236.
Minh, B.Q., Nguyen, M.A.T. & von Haeseler, A. (2013) Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution, 30, 1188-1195.
Moran, N.A. & Bennett, G.M. (2014) The tiniest tiny genomes. Annual Review of Microbiology, 68, 195-215.
Moran, N.A., McCutcheon, J.P. & Nakabachi, A. (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics, 42, 165-190.
Muñoz-Gómez, S.A., 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.
Nguyen, L.-T., Schmidt, H.A., von Haeseler, A. & Minh, B.Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274.
Nunan, L.M., Pantoja, C.R., Gomez-Jimenez, S. & Lightner, D.V. (2013) ‘Candidatus Hepatobacter penaei,’ an intracellular pathogenic enteric bacterium in the Hepatopancreas of the marine shrimp Penaeus vannamei (Crustacea: Decapoda). Applied and Environmental Microbiology, 79, 1407-1409.
Potekhin, A., Nekrasova, I. & Flemming, F. (2021) In shadow of Holospora - the continuous quest for new Holosporaceae members. Protistology, 15, 127-141.
Raymann, K., Bobay, L.-M., Doak, T.G., Lynch, M. & Gribaldo, S. (2013) A genomic survey of Reb homologs suggests widespread occurrence of R-bodies in proteobacteria. G3 (Bethesda, MD), 3, 505-516.
Renvoisé, A., Merhej, V., Georgiades, K. & Raoult, D. (2011) Intracellular Rickettsiales: insights into manipulators of eukaryotic cells. Trends in Molecular Medicine, 17, 573-583.
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. Systematic Biology, 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’. European Journal of Protistology, 62, 79-94.
Sandström, J.P., Russell, J.A., White, J.P. & Moran, N.A. (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Molecular Ecology, 10, 217-228.
Sassera, D., Beninati, T., Epis, S., Bandi, C., Beati, L., Montagna, M. et al. (2010) ‘Candidatus Midichloria mitochondrii’, formerly IricES1, a symbiont of the tick Ixodes ricinus that resides in the host mitochondria. In: Sabelis, M.W. & Bruin, J. (Eds.) Trends in acarology. Dordrecht: Springer Netherlands, pp. 527-531.
Schmitz-Esser, S., Linka, N., Collingro, A., Beier, C.L., Neuhaus, H.E., Wagner, M. et al. (2004) ATP/ADP translocases: a common feature of obligate intracellular Amoebal symbionts related to Chlamydiae and Rickettsiae. Journal of Bacteriology, 186, 683-691.
Schön, M.E., Martijn, J., Vosseberg, J., Köstlbacher, S. & Ettema, T.J.G. (2022) The evolutionary origin of host association in the Rickettsiales. Nature Microbiology, 7, 1189-1199.
Schrallhammer, M., Castelli, M. & Petroni, G. (2018) Phylogenetic relationships among endosymbiotic R-body producer: bacteria providing their host the killer trait. Systematic and Applied Microbiology, 41, 213-220.
Schrallhammer, M., Görtz, H.-D., Ludwig, W., Schleifer, K.-H. & Petroni, G. (2005) Characterization of R-body genetic determinants in Caedibacter caryophilus a symbiont of Paramecium caudatum: preliminary results. The Journal of Eukaryotic Microbiology, 52, 38S-43S.
Schrallhammer, M. & Potekhin, A. (2020) Epidemiology of nucleus-dwelling Holospora: infection, transmission, adaptation, and interaction with paramecium. Results and Problems in Cell Differentiation, 69, 105-135.
Schrallhammer, M. & Schweikert, M. (2009) The killer effect of paramecium and its causative agents. In: Fujishima, M. (Ed.) Endosymbionts in paramecium. Microbiology monographs. Berlin, Heidelberg: Springer, pp. 227-246.
Schulz, F., Lagkouvardos, I., Wascher, F., Aistleitner, K., Kostanjšek, R. & Horn, M. (2014) Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. The ISME Journal, 8, 1634-1644.
Schulz, F., Martijn, J., Wascher, F., Lagkouvardos, I., Kostanjšek, R., Ettema, T.J.G. et al. (2016) A Rickettsiales symbiont of amoebae with ancient features. Environmental Microbiology, 18, 2326-2342.
Seemann, T. (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics, 30, 2068-2069.
Shi, K., Huang, W.M. & Aihara, H. (2013) An enzyme-catalyzed multistep DNA refolding mechanism in hairpin telomere formation. PLoS Biology, 11, e1001472.
Shiohama, Y., Takeshita, K., Hirakata, Y., Nobu, M.K., Ito, M. & Shinzato, N. (2022) Complete genome sequence of ‘Candidatus Hydrogeosomobacter endosymbioticus,’ an intracellular bacterial symbiont of the anaerobic ciliate Scuticociliate GW7. Microbiology Resource Announcements, 11, e01150.
Siewert, L.K., Dehio, C. & Pinschewer, D.D. (2022) Adaptive immune defense prevents Bartonella persistence upon trans-placental transmission. PLoS Pathogens, 18, e1010489.
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.
Stamatakis, A. (2015) Using RAxML to infer phylogenies. Current Protocols in Bioinformatics, 51, 6-14.
Suzuki, H., Dapper, A.L., Jackson, C.E., Lee, H., Pejaver, V., Doak, T.G. et al. (2015) Draft genome sequence of Caedibacter varicaedens, a kappa killer endosymbiont bacterium of the ciliate paramecium biaurelia. Genome Announcements, 3, e01310-e01315.
Szokoli, F., Castelli, M., Sabaneyeva, E., Schrallhammer, M., Krenek, S., Doak, T.G. et al. (2016) 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. Applied and Environmental Microbiology, 82, 7236-7247.
Takeshita, K., Yamada, T., Kawahara, Y., Narihiro, T., Ito, M., Kamagata, Y. et al. (2019) Tripartite symbiosis of an anaerobic Scuticociliate with two Hydrogenosome-associated endosymbionts, a Holospora-related Alphaproteobacterium and a methanogenic archaeon. Applied and Environmental Microbiology, 85, e00854.
Talavera, G. & Castresana, J. (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology, 56, 564-577.
Tashyreva, D., Prokopchuk, G., Votýpka, J., Yabuki, A., Horák, A. & Lukeš, J. (2018) Life cycle, ultrastructure, and phylogeny of new Diplonemids and their endosymbiotic bacteria. mBio, 9, e02447-17.
van Schaik, E.J., Chen, C., Mertens, K., Weber, M.M. & Samuel, J.E. (2013) Molecular pathogenesis of the obligate intracellular bacterium Coxiella burnetii. Nature Reviews. Microbiology, 11, 561-573.
Wang, B., Lin, Y.-C., Vasquez-Rifo, A., Jo, J., Price-Whelan, A., McDonald, S.T. et al. (2021) Pseudomonas aeruginosa PA14 produces R-bodies, extendable protein polymers with roles in host colonization and virulence. Nature Communications, 12, 4613.
Wang, S. & Luo, H. (2021) Dating Alphaproteobacteria evolution with eukaryotic fossils. Nature Communications, 12, 3324.
Wang, Y., Stingl, U., Anton-Erxleben, F., Zimmer, M. & Brune, A. (2004) ‘Candidatus Hepatincola porcellionum’ gen. Nov., sp. nov., a new, stalk-forming lineage of Rickettsiales colonizing the midgut glands of a terrestrial isopod. Archives of Microbiology, 181, 299-304.
Wang, Z. & Wu, M. (2015) An integrated phylogenomic approach toward pinpointing the origin of mitochondria. Scientific Reports, 5, 7949.
Wernegreen, J.J. (2012) Endosymbiosis. Current Biology, 22, R555-R561.
Wick, R.R., Judd, L.M., Gorrie, C.L. & Holt, K.E. (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Computational Biology, 13, e1005595.
Yankovskaya, V., Horsefield, R., Törnroth, S., Luna-Chavez, C., Miyoshi, H., Léger, C. et al. (2003) Architecture of succinate dehydrogenase and reactive oxygen species generation. Science, 299, 700-704.
Zilio, G., Nørgaard, L.S., Petrucci, G., Zeballos, N., Gougat-Barbera, C., Fronhofer, E.A. et al. (2021) Parasitism and host dispersal plasticity in an aquatic model system. Journal of Evolutionary Biology, 34, 1316-1325.