"Candidatus Intestinibacterium parameciiphilum"-member of the "Candidatus Paracaedibacteraceae" family (Alphaproteobacteria, Holosporales) inhabiting the ciliated protist Paramecium.
Bacterial endosymbionts
Ciliate protists
Holosporales
Paracaedibacteraceae
Paramecium
Symbiosis
Journal
International microbiology : the official journal of the Spanish Society for Microbiology
ISSN: 1618-1905
Titre abrégé: Int Microbiol
Pays: Switzerland
ID NLM: 9816585
Informations de publication
Date de publication:
24 Aug 2023
24 Aug 2023
Historique:
received:
13
05
2023
accepted:
02
08
2023
revised:
28
07
2023
medline:
24
8
2023
pubmed:
24
8
2023
entrez:
24
8
2023
Statut:
aheadofprint
Résumé
Protists frequently host diverse bacterial symbionts, in particular those affiliated with the order Holosporales (Alphaproteobacteria). All characterised members of this bacterial lineage have been retrieved in obligate association with a wide range of eukaryotes, especially multiple protist lineages (e.g. amoebozoans, ciliates, cercozoans, euglenids, and nucleariids), as well as some metazoans (especially arthropods and related ecdysozoans). While the genus Paramecium and other ciliates have been deeply investigated for the presence of symbionts, known members of the family "Candidatus Paracaedibacteraceae" (Holosporales) are currently underrepresented in such hosts. Herein, we report the description of "Candidatus Intestinibacterium parameciiphilum" within the family "Candidatus Paracaedibacteraceae", inhabiting the cytoplasm of Paramecium biaurelia. This novel bacterium is almost twice as big as its relative "Candidatus Intestinibacterium nucleariae" from the opisthokont Nuclearia and does not present a surrounding halo. Based on phylogenetic analyses of 16S rRNA gene sequences, we identified six further potential species-level lineages within the genus. Based on the provenance of the respective samples, we investigated the environmental distribution of the representatives of "Candidatus Intestinibacterium" species. Obtained results are consistent with an obligate endosymbiotic lifestyle, with protists, in particular freshwater ones, as hosts. Thus, available data suggest that association with freshwater protists could be the ancestral condition for the members of the "Candidatus Intestinibacterium" genus.
Identifiants
pubmed: 37615902
doi: 10.1007/s10123-023-00414-5
pii: 10.1007/s10123-023-00414-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023. The Author(s).
Références
Amann RI, Binder BJ, Olson RJ et al (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925
pubmed: 2200342
pmcid: 184531
doi: 10.1128/aem.56.6.1919-1925.1990
Baker BJ, Hugenholtz P, Dawson SC, Banfield JF (2003) Extremely acidophilic protists from acid mine drainage host Rickettsiales-lineage endosymbionts that have intervening sequences in their 16S rRNA genes. Appl Environ Microbiol 69:5512–5518
pubmed: 12957940
pmcid: 194945
doi: 10.1128/AEM.69.9.5512-5518.2003
Beisser D, Graupner N, Bock C et al (2017) Comprehensive transcriptome analysis provides new insights into nutritional strategies and phylogenetic relationships of chrysophytes. PeerJ 5:e2832
pubmed: 28097055
pmcid: 5228505
doi: 10.7717/peerj.2832
Beliavskaia AY, Predeus AV, Garushyants SK et al (2020) New intranuclear symbiotic bacteria from macronucleus of Paramecium putrinum—“Candidatus Gortzia Yakutica”. Diversity 12:198
doi: 10.3390/d12050198
Birtles RJ, Rowbotham TJ, Michel R et al (2000) “Candidatus Odyssella thessalonicensis” gen. nov., sp. nov., an obligate intracellular parasite of Acanthamoeba species. Int J Syst Evol Microbiol 50(Pt 1):63–72
pubmed: 10826788
doi: 10.1099/00207713-50-1-63
Boscaro V, Husnik F, Vannini C, Keeling PJ (2019) Symbionts of the ciliate Euplotes : diversity, patterns and potential as models for bacteria–eukaryote endosymbioses. Proc R. Soc B: Biol Sci 286:20190693
doi: 10.1098/rspb.2019.0693
Boscaro V, Holt CC, Van Steenkiste NWL et al (2022) Microbiomes of microscopic marine invertebrates do not reveal signatures of phylosymbiosis. Nat Microbiol 7:810–819
pubmed: 35618773
doi: 10.1038/s41564-022-01125-9
Burki F, Sandin MM, Jamy M (2021) Diversity and ecology of protists revealed by metabarcoding. Curr Biol 31:R1267–R1280
pubmed: 34637739
doi: 10.1016/j.cub.2021.07.066
Castelli M, Lanzoni O, Giovannini M et al (2022a) “Candidatus Gromoviella agglomerans”, a novel intracellular Holosporaceae parasite of the ciliate Paramecium showing marked genome reduction. Environ Microbiol Rep 14:34–49
pubmed: 34766443
doi: 10.1111/1758-2229.13021
Castelli M, Nardi T, Gammuto L et al (2022b) Host association and intracellularity evolved multiple times independently in the Rickettsiales. bioRxiv
Cole JR, Wang Q, Cardenas E et al (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37:D141–D145
pubmed: 19004872
doi: 10.1093/nar/gkn879
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
pubmed: 22847109
pmcid: 4594756
doi: 10.1038/nmeth.2109
Dirren S, Posch T (2016) Promiscuous and specific bacterial symbiont acquisition in the amoeboid genus Nuclearia(Opisthokonta). FEMS Microbiol Ecol 92:fiw105
pubmed: 27199347
doi: 10.1093/femsec/fiw105
Dziallas C, Allgaier M, Monaghan MT, Grossart H-P (2012) Act together—implications of symbioses in aquatic ciliates. Front Microbiol 3:288. https://doi.org/10.3389/fmicb.2012.00288
Fenchel T, Finlay BJ (1991) The biology of free-living anaerobic ciliates. Eur J Protistol 26:201–215
pubmed: 23196279
doi: 10.1016/S0932-4739(11)80143-4
Flemming FE, Grosser K, Schrallhammer M (2021) Natural shifts in endosymbionts’ occurrence and relative frequency in their ciliate host population. Front Microbiol 12:791615
pubmed: 35087493
doi: 10.3389/fmicb.2021.791615
Foissner W, Hawksworth DL (2009) Protist diversity and geographical distribution. Springer Science & Business Media. https://doi.org/10.1007/978-90-481-2801-3
Fokin SI (2010) Paramecium genus: biodiversity, some morphological features and the key to the main morphospecies discrimination. Protistology 16:227–235
Fokin SI, Serra V (2022) Bacterial symbiosis in ciliates (Alveolata, Ciliophora): roads traveled and those still to be taken. J Eukaryot Microbiol 69:e12886
pubmed: 35006645
pmcid: 9539572
doi: 10.1111/jeu.12886
Fokin SI, Serra V, Ferrantini F et al (2019) “Candidatus Hafkinia simulans” gen. nov., sp. nov., a novel Holospora-like bacterium from the macronucleus of the rare brackish water ciliate Frontonia salmastra (Oligohymenophorea, Ciliophora): multidisciplinary characterization of the new endosymbiont and its host. Microb Ecol 77:1092–1106
pubmed: 30627761
doi: 10.1007/s00248-018-1311-0
Fraune S, Bosch TCG (2007) Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proc Natl Acad Sci U S A 104:13146–13151
pubmed: 17664430
pmcid: 1934924
doi: 10.1073/pnas.0703375104
García-Moyano A, González-Toril E, Aguilera Á, Amils R (2012) Comparative microbial ecology study of the sediments and the water column of the Río Tinto, an extreme acidic environment. FEMS Microbiol Ecol 81:303–314
pubmed: 22385317
doi: 10.1111/j.1574-6941.2012.01346.x
Garushyants SK, Beliavskaia AY, Malko DB et al (2018) Comparative genomic analysis of spp., intranuclear symbionts of Paramecia. Front Microbiol 9:738
pubmed: 29713316
pmcid: 5911502
doi: 10.3389/fmicb.2018.00738
Gast RJ, Sanders RW, Caron DA (2009) Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol 17:563–569
pubmed: 19828317
doi: 10.1016/j.tim.2009.09.001
Gihring TM, Moser DP, Lin L-H et al (2006) The distribution of microbial taxa in the subsurface water of the Kalahari shield, South Africa. Geomicrobiol J 23:415–430
doi: 10.1080/01490450600875696
Gomez-Alvarez V, Humrighouse BW, Revetta RP, Santo Domingo JW (2015) Bacterial composition in a metropolitan drinking water distribution system utilizing different source waters. J Water Health 13:140–151
pubmed: 25719474
doi: 10.2166/wh.2014.057
Görtz H-D, Fokin SI (2009) Diversity of endosymbiotic bacteria in Paramecium. In: Fujishima M (ed) Endosymbionts in Paramecium 131–160. Springer-Verlag, Berlin-Heidelberg
Graf JS, Schorn S, Kitzinger K et al (2021) Anaerobic endosymbiont generates energy for ciliate host by denitrification. Nature 591:445–450
pubmed: 33658719
pmcid: 7969357
doi: 10.1038/s41586-021-03297-6
Grice EA, Kong HH, Conlan S et al (2009) Topographical and temporal diversity of the human skin microbiome. Science 324:1190–1192
pubmed: 19478181
pmcid: 2805064
doi: 10.1126/science.1171700
Guidetti R, Vecchi M, Ferrari A et al (2020) Further insights in the Tardigrada microbiome: phylogenetic position and prevalence of infection of four new Alphaproteobacteria putative endosymbionts. Zool J Linn Soc 188:925–937
doi: 10.1093/zoolinnean/zlz128
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704
pubmed: 14530136
doi: 10.1080/10635150390235520
Headd B, Engel AS (2014) Biogeographic congruency among bacterial communities from terrestrial sulfidic springs. Front Microbiol 5:473
pubmed: 25250021
pmcid: 4157610
doi: 10.3389/fmicb.2014.00473
Hess S, Suthaus A, Melkonian M (2016) “Candidatus Finniella” (Rickettsiales, Alphaproteobacteria), novel endosymbionts of Viridiraptorid Amoeboflagellates (Cercozoa, Rhizaria). Appl Environ Microbiol 82:659–670
pubmed: 26567303
pmcid: 4711129
doi: 10.1128/AEM.02680-15
Hirakata Y, Oshiki M, Kuroda K et al (2015) Identification and detection of prokaryotic symbionts in the ciliate Metopus from anaerobic granular sludge. Microbes Environ 30:335–338
pubmed: 26639580
pmcid: 4676557
doi: 10.1264/jsme2.ME15154
Hongoh Y, Ohkuma M, Kudo T (2003) Molecular analysis of bacterial microbiota in the gut of the termite Reticulitermes speratus (Isoptera; Rhinotermitidae). FEMS Microbiol Ecol 44:231–242
pubmed: 19719640
doi: 10.1016/S0168-6496(03)00026-6
Horn M, Fritsche TR, Gautom RK et al (1999) Novel bacterial endosymbionts of Acanthamoeba spp. related to the Paramecium caudatum symbiont Caedibacter caryophilus. Environ Microbiol 1:357–367
pubmed: 11207753
doi: 10.1046/j.1462-2920.1999.00045.x
Husnik F, Tashyreva D, Boscaro V et al (2021) Bacterial and archaeal symbioses with protists. Curr Biol 31:R862–R877
pubmed: 34256922
doi: 10.1016/j.cub.2021.05.049
Jogler M, Siemens H, Chen H et al (2011) Identification and targeted cultivation of abundant novel freshwater sphingomonads and analysis of their population substructure. Appl Environ Microbiol 77:7355–7364
pubmed: 21873487
pmcid: 3194862
doi: 10.1128/AEM.05832-11
Kim E, Park JS, Simpson AGB et al (2010) Complex array of endobionts in Petalomonas sphagnophila, a large heterotrophic euglenid protist from Sphagnum-dominated peatlands. ISME J 4:1108–1120
pubmed: 20376101
doi: 10.1038/ismej.2010.40
Kim L, Pagaling E, Zuo YY, Yan T (2014a) Impact of substratum surface on microbial community structure and treatment performance in biological aerated filters. Appl Environ Microbiol 80:177–183
pubmed: 24141134
pmcid: 3911025
doi: 10.1128/AEM.03001-13
Kim M, Oh H-S, Park S-C, Chun J (2014b) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351
pubmed: 24505072
doi: 10.1099/ijs.0.059774-0
Konecka E, Olszanowski Z (2019) Detection of a new bacterium of the family Holosporaceae (Alphaproteobacteria: Holosporales) associated with the oribatid mite Achipteria coleoptrata. Biologia 74:1517–1522
doi: 10.2478/s11756-019-00251-w
Krenek S, Berendonk TU, Petzoldt T (2011) Thermal performance curves of Paramecium caudatum: a model selection approach. Eur J Protistol 47:124–137
pubmed: 21277756
doi: 10.1016/j.ejop.2010.12.001
Kroer P, Kjeldsen KU, Nyengaard JR et al (2016) A novel extracellular gut symbiont in the marine worm Priapulus caudatus (Priapulida) reveals an alphaproteobacterial symbiont clade of the Ecdysozoa. Front Microbiol 7:539. https://doi.org/10.3389/fmicb.2016.00539
Lagkouvardos I, Joseph D, Kapfhammer M et al (2016) IMNGS: a comprehensive open resource of processed 16S rRNA microbial profiles for ecology and diversity studies. Sci Rep 6:33721
pubmed: 27659943
pmcid: 5034312
doi: 10.1038/srep33721
Lanzoni O, Fokin SI, Lebedeva N et al (2016) Rare freshwater ciliate Paramecium chlorelligerum Kahl, 1935 and its macronuclear symbiotic bacterium “Candidatus Holospora parva”. PloS One 11:e0167928
pubmed: 27992463
pmcid: 5161471
doi: 10.1371/journal.pone.0167928
Lanzoni O, Sabaneyeva EV, Modeo L et al (2019) Diversity and environmental distribution of the cosmopolitan endosymbiont “Candidatus Megaira”. Sci Reports 9(1):1179. https://doi.org/10.1038/s41598-018-37629-w
Ludwig W, Strunk O, Westram R et al (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32:1363–1371
pubmed: 14985472
pmcid: 390282
doi: 10.1093/nar/gkh293
Magaña ML, Fernández-Díez J, Magaña M (2008) Cutaneous amebiasis in pediatrics. Arch Dermatol 144:1369–1372
pubmed: 18936402
doi: 10.1001/archderm.144.10.1369
Marshall Hathaway JJ, Garcia MG, Balasch MM et al (2014) Comparison of bacterial diversity in Azorean and Hawai’ian lava cave microbial mats. Geomicrobiol J 31:205–220
pubmed: 26924866
pmcid: 4765387
doi: 10.1080/01490451.2013.777491
Martijn J, Vosseberg J, Guy L et al (2018) Deep mitochondrial origin outside the sampled alphaproteobacteria. Nature 557:101–105
pubmed: 29695865
doi: 10.1038/s41586-018-0059-5
McFall-Ngai M, Hadfield MG, Bosch TCG et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236
pubmed: 23391737
pmcid: 3587249
doi: 10.1073/pnas.1218525110
Midha S, Rigden DJ, Siozios S et al (2021) Bodo saltans (Kinetoplastida) is dependent on a novel Paracaedibacter-like endosymbiont that possesses multiple putative toxin-antitoxin systems. ISME J 15:1680–1694
pubmed: 33452479
pmcid: 8163844
doi: 10.1038/s41396-020-00879-6
Modeo L, Fokin SI, Boscaro V et al (2013) Morphology, ultrastructure, and molecular phylogeny of the ciliate Sonderia vorax with insights into the systematics of order Plagiopylida. BMC Microbiol 13:40
pubmed: 23418998
pmcid: 3626617
doi: 10.1186/1471-2180-13-40
Morán P, Rojas L, Cerritos R et al (2013) Case report: cutaneous amebiasis: the importance of molecular diagnosis of an emerging parasitic disease. Am J Trop Med Hyg 88:186–190
pubmed: 23208883
pmcid: 3541734
doi: 10.4269/ajtmh.2012.12-0278
Muñoz-Gómez SA, Hess S, Burger G et al (2019) An updated phylogeny of the Alphaproteobacteria reveals that the parasitic Rickettsiales and Holosporales have independent origins. eLife 8:e42535. https://doi.org/10.7554/eLife.42535
Muñoz-Gómez SA, Kreutz M, Hess S (2021) A microbial eukaryote with a unique combination of purple bacteria and green algae as endosymbionts. Sci Adv 7. https://doi.org/10.1126/sciadv.abg4102
Nitla V, Serra V, Fokin SI et al (2019) Critical revision of the family Plagiopylidae (Ciliophora: Plagiopylea), including the description of two novel species, Plagiopyla ramani and Plagiopyla narasimhamurtii, and redescription of Plagiopyla nasuta Stein, 1860 from India. Zool J Linn Soc 186:1–45
doi: 10.1093/zoolinnean/zly041
Nogueira T, Botelho A, Bowler L, Inácio J (2022) Editorial: Evolution of animal microbial communities in response to environmental stress. Front Microbiol 13:860609
pubmed: 35432293
pmcid: 9005952
doi: 10.3389/fmicb.2022.860609
Nowack ECM, Melkonian M (2010) Endosymbiotic associations within protists. Philos Trans R Soc Lond B Biol Sci 365:699–712
pubmed: 20124339
pmcid: 2817226
doi: 10.1098/rstb.2009.0188
Nunan LM, Pantoja CR, Gomez-Jimenez S, Lightner DV (2013) “Candidatus Hepatobacter penaei” an Intracellular Pathogenic Enteric Bacterium in the Hepatopancreas of the Marine Shrimp Penaeus vannamei (Crustacea: Decapoda). Appl Environ Microbiol 79:1407–1409
pubmed: 23241970
pmcid: 3568585
doi: 10.1128/AEM.02425-12
Oliverio AM, Geisen S, Delgado-Baquerizo M et al (2020) The global-scale distributions of soil protists and their contributions to belowground systems. Sci Adv 6:eaax8787
pubmed: 32042898
pmcid: 6981079
doi: 10.1126/sciadv.aax8787
Oren A, Garrity GM, Parker CT, Chuvochina M, Trujillo ME (2020) Lists of names of prokaryotic Candidatus taxa. Int J Syst Evol Microbiol 70:3956–4042. https://doi.org/10.1099/ijsem.0.003789
Potekhin A, Schweikert M, Nekrasova I et al (2018) Complex life cycle, broad host range and adaptation strategy of the intranuclear Paramecium symbiont Preeria caryophila comb. nov. FEMS Microbiol Ecol 94. https://doi.org/10.1093/femsec/fiy076
Prieto-Granada CN, Lobo AZC, Mihm MC Jr (2010) Skin infections. In: Kradin RL (ed) Diagnostic pathology of infectious disease. Elsevier, pp 519–616. https://doi.org/10.1016/B978-1-4160-3429-2.00019-5
doi: 10.1016/B978-1-4160-3429-2.00019-5
Quast C, Pruesse E, Yilmaz P et al (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596
pubmed: 23193283
doi: 10.1093/nar/gks1219
Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
pubmed: 22357727
pmcid: 3329765
doi: 10.1093/sysbio/sys029
Sabaneyeva E, Castelli M, Szokoli F et al (2018) Host and symbiont intraspecific variability: the case of Paramecium calkinsi and “Candidatus Trichorickettsia mobilis”. Eur J Protistol 62:79–94
pubmed: 29287245
doi: 10.1016/j.ejop.2017.12.002
Santofimia E, González-Toril E, López-Pamo E et al (2013) Microbial diversity and its relationship to physicochemical characteristics of the water in two extreme acidic pit lakes from the Iberian Pyrite Belt (SW Spain). PloS One 8:e66746
pubmed: 23840525
pmcid: 3694112
doi: 10.1371/journal.pone.0066746
Scheid P (2014) Relevance of free-living amoebae as hosts for phylogenetically diverse microorganisms. Parasitol Res 113:2407–2414
pubmed: 24828345
doi: 10.1007/s00436-014-3932-7
Schön ME, Martijn J, Vosseberg J et al (2022) The evolutionary origin of host association in the Rickettsiales. Nat Microbiol 7:1189–1199
pubmed: 35798888
pmcid: 9352585
doi: 10.1038/s41564-022-01169-x
Schrallhammer M, Potekhin A (2020) Epidemiology of nucleus-dwelling Holospora: infection, transmission, adaptation, and interaction with Paramecium. Results Probl Cell Differ 69:105–135
pubmed: 33263870
doi: 10.1007/978-3-030-51849-3_4
Schrallhammer M, Schweikert M (2009) The killer effect of Paramecium and its causative agents. In: Fujishima M (ed) Endosymbionts in Paramecium. Springer, Berlin Heidelberg, pp 227–246. https://doi.org/10.1007/978-3-540-92677-1_9
Schrallhammer M, Castelli M, Petroni G (2018) Phylogenetic relationships among endosymbiotic R-body producer: bacteria providing their host the killer trait. Syst Appl Microbiol 41:213–220
pubmed: 29426636
doi: 10.1016/j.syapm.2018.01.005
Schulz F, Lagkouvardos I, Wascher F et al (2014) Life in an unusual intracellular niche: a bacterial symbiont infecting the nucleus of amoebae. ISME J 8:1634–1644
pubmed: 24500618
pmcid: 4817620
doi: 10.1038/ismej.2014.5
Schuster L, Bright M (2016) A novel colonial ciliate Zoothamnium ignavum sp. nov. (Ciliophora, Oligohymenophorea) and its ectosymbiont Candidatus Navis piranensis gen. nov., sp. nov. from shallow-water wood falls. PloS One 11:e0162834
pubmed: 27683199
pmcid: 5040259
doi: 10.1371/journal.pone.0162834
Serra V, Gammuto L, Nitla V 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. https://doi.org/10.1038/s41598-020-76348-z
Shaw AK, Halpern AL, Beeson K et al (2008) It’s all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10:2200–2210
pubmed: 18637951
doi: 10.1111/j.1462-2920.2008.01626.x
Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited : tarnished gold standards. Microbiol Today 4:152–155
Szokoli F, Castelli M, Sabaneyeva E 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
pubmed: 27742680
pmcid: 5118934
doi: 10.1128/AEM.02284-16
Szokoli F, Sabaneyeva E, Castelli M et al (2016b) “Candidatus Fokinia solitaria”, a novel “stand-alone” symbiotic lineage of Midichloriaceae (Rickettsiales). PloS One 11:e0145743
pubmed: 26731731
pmcid: 4701390
doi: 10.1371/journal.pone.0145743
Takeshita K, Yamada T, Kawahara Y et al (2019) Tripartite symbiosis of an anaerobic scuticociliate with two hydrogenosome-associated endosymbionts, a Holospora-related alphaproteobacterium and a methanogenic archaeon. Appl Environ Microbiol 85:e00854-19. https://doi.org/10.1128/AEM.00854-19
Tashyreva D, Prokopchuk G, Votýpka J et al (2018) Life cycle, ultrastructure, and phylogeny of new diplonemids and their endosymbiotic bacteria. MBio 9:e02447-17. https://doi.org/10.1128/mBio.02447-17
Vannini C, Petroni G, Verni F, Rosati G (2005) A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Microb Ecol 49:434–442
pubmed: 16003470
doi: 10.1007/s00248-004-0055-1
van Rensburg JJ, Lin H, Gao X et al (2015) The human skin microbiome associates with the outcome of and is influenced by bacterial infection. MBio 6:e01315–e01315
pubmed: 26374122
pmcid: 4600114
Wang S, Luo H (2021) Dating Alphaproteobacteria evolution with eukaryotic fossils. Nat Commun 12:3324
pubmed: 34083540
pmcid: 8175736
doi: 10.1038/s41467-021-23645-4
Wang Y, Stingl U, Anton-Erxleben F et al (2004) “Candidatus Hepatincola porcellionum” gen. nov., sp. nov., a new, stalk-forming lineage of Rickettsiales colonizing the midgut glands of a terrestrial isopod. Arch Microbiol 181:299–304
pubmed: 14770277
doi: 10.1007/s00203-004-0655-7
Weinert LA, Werren JH, Aebi A et al (2009) Evolution and diversity of Rickettsia bacteria. BMC Biol 7:6
pubmed: 19187530
pmcid: 2662801
doi: 10.1186/1741-7007-7-6
Yarza P, Yilmaz P, Pruesse E et al (2014) Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 12:635–645
pubmed: 25118885
doi: 10.1038/nrmicro3330
Yuhana M, Horath T, Hanselmann K (2006) Bacterial community shifts of a high mountain lake in response to variable simulated conditions: availability of nutrients, light and oxygen. Biotropia - The Southeast Asian Journal of Tropical Biology 13. https://doi.org/10.11598/btb.2006.13.2.219
Zaila KE, Doak TG, Ellerbrock H et al (2017) Diversity and universality of endosymbiotic Rickettsia in the fish parasite Ichthyophthirius multifiliis. Front Microbiol 8:189
pubmed: 28232825
pmcid: 5299013
doi: 10.3389/fmicb.2017.00189
Zhao Z, Jiang J, Zheng J et al (2022) Exploiting the gut microbiota to predict the origins and quality traits of cultured sea cucumbers. Environ Microbiol 24:3882–3897
pubmed: 35297145
doi: 10.1111/1462-2920.15972
Zilio G, Nørgaard LS, Petrucci G et al (2021) Parasitism and host dispersal plasticity in an aquatic model system. J Evol Biol 34:1316–1325
pubmed: 34157176
doi: 10.1111/jeb.13893