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The terrestrial isopod symbiont ‘Candidatus Hepatincola porcellionum’ is a potential nutrient scavenger related to Holosporales symbionts of protists

  • McCutcheon JP, Boyd BM, Dale C. The life of an insect endosymbiont from the cradle to the grave. Curr Biol. 2019;29:R485–95.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • McCutcheon JP, Moran NA. Extreme genome reduction in symbiotic bacteria. Nat Rev Microbiol. 2012;10:13–26.

    Article 
    CAS 

    Google Scholar 

  • Latorre A, Manzano-Marin A. Dissecting genome reduction and trait loss in insect endosymbionts. Ann N Y Acad Sci. 2017;1389:52–75.

    Article 
    PubMed 

    Google Scholar 

  • Salje J. Cells within cells: Rickettsiales and the obligate intracellular bacterial lifestyle. Nat Rev Microbiol. 2021;19:375–90.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kaur R, Shropshire JD, Cross KL, Leigh B, Mansueto AJ, Stewart V, et al. Living in the endosymbiotic world of Wolbachia: a centennial review. Cell Host Microbe. 2021;29:879–93.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pilgrim J, Thongprem P, Davison HR, Siozios S, Baylis M, Zakharov EV, et al. Torix Rickettsia are widespread in arthropods and reflect a neglected symbiosis. Gigascience. 2021;10:giab021.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pilgrim J, Ander M, Garros C, Baylis M, Hurst GDD, Siozios S. Torix group Rickettsia are widespread in Culicoides biting midges (Diptera: Ceratopogonidae), reach high frequency and carry unique genomic features. Environ Microbiol. 2017;19:4238–55.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Horn M, Fritsche TR, Gautom RK, Schleifer KH, Wagner M. Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol. 1999;1:357–67.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Schulz F, Lagkouvardos I, Wascher F, Aistleitner K, Kostanjsek R, Horn M. Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. ISME J. 2014;8:1634–44.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schulz F, Martijn J, Wascher F, Lagkouvardos I, Kostanjsek R, Ettema TJ, et al. A Rickettsiales symbiont of amoebae with ancient features. Environ Microbiol. 2016;18:2326–42.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Hess S, Suthaus A, Melkonian M. “Candidatus Finniella” (Rickettsiales, Alphaproteobacteria), Novel Endosymbionts of Viridiraptorid Amoeboflagellates (Cercozoa, Rhizaria). Appl Environ Microbiol. 2016;82:659–70.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Castelli M, Sabaneyeva E, Lanzoni O, Lebedeva N, Floriano AM, Gaiarsa S, et al. Deianiraea, an extracellular bacterium associated with the ciliate Paramecium, suggests an alternative scenario for the evolution of Rickettsiales. ISME J. 2019;13:2280–94.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Floriano AM, Castelli M, Krenek S, Berendonk TU, Bazzocchi C, Petroni G, et al. The genome sequence of “Candidatus Fokinia solitaria”: insights on reductive evolution in Rickettsiales. Genome Biol Evol. 2018;10:1120–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • George EE, Husnik F, Tashyreva D, Prokopchuk G, Horak A, Kwong WK, et al. Highly reduced genomes of protist endosymbionts show evolutionary convergence. Curr Biol. 2020;30:925–33.e3.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Midha S, Rigden DJ, Siozios S, Hurst GDD, Jackson AP. Bodo saltans (Kinetoplastida) is dependent on a novel Paracaedibacter-like endosymbiont that possesses multiple putative toxin-antitoxin systems. ISME J. 2021;15:1680–94.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Castelli M, Lanzoni O, Giovannini M, Lebedeva N, Gammuto L, Sassera D, et al. ‘Candidatus Gromoviella agglomerans’, a novel intracellular Holosporaceae parasite of the ciliate Paramecium showing marked genome reduction. Environ Microbiol Rep. 2022;14:34–49.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Klinges JG, Rosales SM, McMinds R, Shaver EC, Shantz AA, Peters EC, et al. Phylogenetic, genomic, and biogeographic characterization of a novel and ubiquitous marine invertebrate-associated Rickettsiales parasite, Candidatus Aquarickettsia rohweri, gen. nov., sp. nov. ISME J. 2019;13:2938–53.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kroer P, Kjeldsen KU, Nyengaard JR, Schramm A, Funch P. A novel extracellular gut symbiont in the marine worm Priapulus caudatus (Priapulida) reveals an Alphaproteobacterial symbiont clade of the ecdysozoa. Front Microbiol. 2016;7:539.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yurchenko T, Sevcikova T, Pribyl P, El Karkouri K, Klimes V, Amaral R, et al. A gene transfer event suggests a long-term partnership between eustigmatophyte algae and a novel lineage of endosymbiotic bacteria. ISME J. 2018;12:2163–75.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ferla MP, Thrash JC, Giovannoni SJ, Patrick WM. New rRNA gene-based phylogenies of the Alphaproteobacteria provide perspective on major groups, mitochondrial ancestry and phylogenetic instability. PLoS ONE. 2013;8:e83383.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Szokoli F, Castelli M, Sabaneyeva E, Schrallhammer M, Krenek S, Doak TG, et al. 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. 2016;82:7236–47.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Munoz-Gomez SA, Hess S, Burger G, Lang BF, Susko E, Slamovits CH, et al. An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. eLife. 2019;8:e42535.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sassera D, Beninati T, Bandi C, Bouman EA, Sacchi L, Fabbi M, et al. ‘Candidatus Midichloria mitochondrii’, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Syst Evol Microbiol. 2006;56:2535–40.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Fokin SI, Görtz HD, Diversity of Holospora bacteria in Paramecium and their characterization. In: Fujishima M, editor. Endosymbionts in Paramecium. Microbiology Monographs, vol 12. Berlin: Springer; 2009. https://doi.org/10.1007/978-3-540-92677-1_7.

  • Min CK, Yang JS, Kim S, Choi MS, Kim IS, Cho NH. Genome-based construction of the metabolic pathways of Orientia tsutsugamushi and comparative analysis within the Rickettsiales order. Comp Funct Genomics. 2008;2008:623145.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Garushyants SK, Beliavskaia AY, Malko DB, Logacheva MD, Rautian MS, Gelfand MS. Comparative genomic analysis of Holospora spp., intranuclear symbionts of paramecia. Front Microbiol. 2018;9:738.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Boscaro V, Fokin SI, Schrallhammer M, Schweikert M, Petroni G. Revised systematics of Holospora-like bacteria and characterization of “Candidatus Gortzia infectiva”, a novel macronuclear symbiont of Paramecium jenningsi. Microb Ecol. 2013;65:255–67.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Serra V, Fokin SI, Castelli M, Basuri CK, Nitla V, Verni F, et al. “Candidatus Gortzia shahrazadis”, a novel endosymbiont of Paramecium multimicronucleatum and a revision of the biogeographical distribution of Holospora-like bacteria. Front Microbiol. 2016;7:1704.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Takeshita K, Yamada T, Kawahara Y, Narihiro T, Ito M, Kamagata Y, et al. Tripartite symbiosis of an anaerobic scuticociliate with two hydrogenosome-associated endosymbionts, a Holospora-related Alphaproteobacterium and a Methanogenic Archaeon. Appl Environ Microbiol. 2019;85:e00854–19.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang Y, Brune A, Zimmer M. Bacterial symbionts in the hepatopancreas of isopods: diversity and environmental transmission. FEMS Microbiol Ecol. 2007;61:141–52.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wang Y, Stingl U, Anton-Erxleben F, Zimmer M, Brune A. ‘Candidatus Hepatincola porcellionum’ gen. nov., sp. nov., a new, stalk-forming lineage of Rickettsiales colonizing the midgut glands of a terrestrial isopod. Arch Microbiol. 2004;181:299–304.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Fraune S, Zimmer M. Host-specificity of environmentally transmitted Mycoplasma-like isopod symbionts. Environ Microbiol. 2008;10:2497–504.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Dittmer J, Lesobre J, Moumen B, Bouchon D. Host origin and tissue microhabitat shaping the microbiota of the terrestrial isopod Armadillidium vulgare. FEMS Microbiol Ecol. 2016;92:fiw063.

    Article 
    PubMed 

    Google Scholar 

  • Zimmer M, Topp W. Microorganisms and cellulose digestion in the gut of the woodlouse Porcellio scaber. J Chem Ecol. 1998;24:1397–408.

    Article 
    CAS 

    Google Scholar 

  • Zimmer M, Danko JP, Pennings SC, Danford AR, Ziegler A, Uglow RF, et al. Hepatopancreatic endosymbionts in coastal isopods (Crustacea: Isopoda), and their contribution to digestion. Mar Biol. 2001;138:955–63.

    Article 

    Google Scholar 

  • Bouchon D, Zimmer M, Dittmer J. The terrestrial isopod microbiome: an all-in-one toolbox for animal-microbe interactions of ecological relevance. Front Microbiol. 2016;7:1472.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Dittmer J, Beltran-Bech S, Lesobre J, Raimond M, Johnson M, Bouchon D. Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods. Mol Ecol. 2014;23:2619–35.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–100.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27:722–36.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Loman NJ, Quick J, Simpson JT. A complete bacterial genome assembled de novo using only nanopore sequencing data. Nat Methods. 2015;12:733–5.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Vaser R, Sovic I, Nagarajan N, Sikic M. Fast and accurate de novo genome assembly from long uncorrected reads. Genome Res. 2017;27:737–46.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wick RR, Holt KE. Polypolish: short-read polishing of long-read bacterial genome assemblies. PLoS Comput Biol. 2022;18:e1009802.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bredon M, Dittmer J, Noel C, Moumen B, Bouchon D. Lignocellulose degradation at the holobiont level: teamwork in a keystone soil invertebrate. Microbiome. 2018;6:162.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bredon M, Herran B, Bertaux J, Greve P, Moumen B, Bouchon D. Isopod holobionts as promising models for lignocellulose degradation. Biotechnol Biofuels. 2020;13:49.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Li D, Liu CM, Luo R, Sadakane K, Lam TW. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics. 2015;31:1674–6.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Kang DD, Li F, Kirton E, Thomas A, Egan R, An H, et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ. 2019;7:e7359.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25:1043–55.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res. 2007;35:3100–8.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Prjibelski A, Antipov D, Meleshko D, Lapidus A, Korobeynikov A. Using SPAdes de novo assembler. Curr Protoc Bioinformatics. 2020;70:e102.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Darling AC, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14:1394–403.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Badawi M, Moumen B, Giraud I, Greve P, Cordaux R. Investigating the molecular genetic basis of cytoplasmic sex determination caused by Wolbachia endosymbionts in terrestrial isopods. Genes. 2018;9:290.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wick RR, Judd LM, Gorrie CL, Holt KE. Completing bacterial genome assemblies with multiplex MinION sequencing. Microb Genom. 2017;3:e000132.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kolmogorov M, Bickhart DM, Behsaz B, Gurevich A, Rayko M, Shin SB, et al. metaFlye: scalable long-read metagenome assembly using repeat graphs. Nat Methods. 2020;17:1103–10.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Mistry J, Chuguransky S, Williams L, Qureshi M, Salazar GA, Sonnhammer ELL, et al. Pfam: the protein families database in 2021. Nucleic Acids Res. 2021;49:D412–9.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32:W327–31.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Carver T, Harris SR, Berriman M, Parkhill J, McQuillan JA. Artemis: an integrated platform for visualization and analysis of high-throughput sequence-based experimental data. Bioinformatics. 2012;28:464–9.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31:3210–2.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Eren AM, Kiefl E, Shaiber A, Veseli I, Miller SE, Schechter MS, et al. Community-led, integrated, reproducible multi-omics with anvi’o. Nat Microbiol. 2021;6:3–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cantalapiedra CP, Hernandez-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021;38:5825–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Abby SS, Cury J, Guglielmini J, Neron B, Touchon M, Rocha EP. Identification of protein secretion systems in bacterial genomes. Sci Rep. 2016;6:23080.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Teufel F, Almagro Armenteros JJ, Johansen AR, Gislason MH, Pihl SI, Tsirigos KD, et al. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nat Biotechnol. 2022;40:1023–5.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Elbourne LD, Tetu SG, Hassan KA, Paulsen IT. TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life. Nucleic Acids Res. 2017;45:D320–4.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, et al. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res. 2021;49:W29–35.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lombard V, Golaconda Ramulu H, Drula E, Coutinho PM, Henrissat B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014;42:D490–5.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Zhang H, Yohe T, Huang L, Entwistle S, Wu P, Yang Z, et al. dbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 2018;46:W95–101.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Arndt D, Grant JR, Marcu A, Sajed T, Pon A, Liang Y, et al. PHASTER: a better, faster version of the PHAST phage search tool. Nucleic Acids Res. 2016;44:W16–21.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chernomor O, von Haeseler A, Minh BQ. Terrace aware data structure for phylogenomic inference from supermatrices. Syst Biol. 2016;65:997–1008.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41:D590–6.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49:W293–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schrallhammer M, Castelli M, Petroni G. Phylogenetic relationships among endosymbiotic R-body producer: bacteria providing their host the killer trait. Syst Appl Microbiol. 2018;41:213–20.

    Article 
    PubMed 

    Google Scholar 

  • Gillespie JJ, Kaur SJ, Rahman MS, Rennoll-Bankert K, Sears KT, Beier-Sexton M, et al. Secretome of obligate intracellular Rickettsia. FEMS Microbiol Rev. 2015;39:47–80.

    CAS 
    PubMed 

    Google Scholar 


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