Revised Systematics of Holospora-like Bacteria and Characterization of "Candidatus Gortzia Infectiva", a Novel Macronuclear Symbiont of Paramecium Jenningsi

Overview

Journal Microb Ecol

Specialties Environmental Health
Microbiology

Date 2012 Sep 4

PMID 22940732

Citations 30

Authors

Vittorio Boscaro

Sergei I Fokin

Martina Schrallhammer

Michael Schweikert

Giulio Petroni

Affiliations

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Abstract

The genus Holospora (Rickettsiales) includes highly infectious nuclear symbionts of the ciliate Paramecium with unique morphology and life cycle. To date, nine species have been described, but a molecular characterization is lacking for most of them. In this study, we have characterized a novel Holospora-like bacterium (HLB) living in the macronuclei of a Paramecium jenningsi population. This bacterium was morphologically and ultrastructurally investigated in detail, and its life cycle and infection capabilities were described. We also obtained its 16S rRNA gene sequence and developed a specific probe for fluorescence in situ hybridization experiments. A new taxon, "Candidatus Gortzia infectiva", was established for this HLB according to its unique characteristics and the relatively low DNA sequence similarities shared with other bacteria. The phylogeny of the order Rickettsiales based on 16S rRNA gene sequences has been inferred, adding to the available data the sequence of the novel bacterium and those of two Holospora species (Holospora obtusa and Holospora undulata) characterized for the purpose. Our phylogenetic analysis provided molecular support for the monophyly of HLBs and showed a possible pattern of evolution for some of their features. We suggested to classify inside the family Holosporaceae only HLBs, excluding other more distantly related and phenotypically different Paramecium endosymbionts.

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References

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(4):299-304. DOI: 10.1007/s00203-004-0655-7. View

Posada D . jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008; 25(7):1253-6. DOI: 10.1093/molbev/msn083. View

Vannini C, Pockl M, Petroni G, Wu Q, Lang E, Stackebrandt E . Endosymbiosis in statu nascendi: close phylogenetic relationship between obligately endosymbiotic and obligately free-living Polynucleobacter strains (Betaproteobacteria). Environ Microbiol. 2007; 9(2):347-59. DOI: 10.1111/j.1462-2920.2006.01144.x. View

Hori M, Fujishima M . The endosymbiotic bacterium Holospora obtusa enhances heat-shock gene expression of the host Paramecium caudatum. J Eukaryot Microbiol. 2004; 50(4):293-8. DOI: 10.1111/j.1550-7408.2003.tb00137.x. View

Murray R, Schleifer K . Taxonomic notes: a proposal for recording the properties of putative taxa of procaryotes. Int J Syst Bacteriol. 1994; 44(1):174-6. DOI: 10.1099/00207713-44-1-174. View

Preer L . Alpha, an infectious macronuclear symbiont of Paramecium aurelia. J Protozool. 1969; 16(3):570-8. DOI: 10.1111/j.1550-7408.1969.tb02315.x. View

Petroni G, Spring S, Schleifer K, Verni F, Rosati G . Defensive extrusive ectosymbionts of Euplotidium (Ciliophora) that contain microtubule-like structures are bacteria related to Verrucomicrobia. Proc Natl Acad Sci U S A. 2000; 97(4):1813-7. PMC: 26518. DOI: 10.1073/pnas.030438197. View

Murray R, Stackebrandt E . Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol. 1995; 45(1):186-7. DOI: 10.1099/00207713-45-1-186. View

Springer N, Ludwig W, Amann R, Schmidt H, Gortz H, Schleifer K . Occurrence of fragmented 16S rRNA in an obligate bacterial endosymbiont of Paramecium caudatum. Proc Natl Acad Sci U S A. 1993; 90(21):9892-5. PMC: 47678. DOI: 10.1073/pnas.90.21.9892. View

10.

Loy A, Maixner F, Wagner M, Horn M . probeBase--an online resource for rRNA-targeted oligonucleotide probes: new features 2007. Nucleic Acids Res. 2006; 35(Database issue):D800-4. PMC: 1669758. DOI: 10.1093/nar/gkl856. View

11.

Gortz H, Lellig S, Miosga O, Wiemann M . Changes in fine structure and polypeptide pattern during development of Holospora obtusa, a bacterium infecting the macronucleus of Paramecium caudatum. J Bacteriol. 1990; 172(10):5664-9. PMC: 526880. DOI: 10.1128/jb.172.10.5664-5669.1990. View

12.

Vannini C, Petroni G, Verni F, Rosati G . A bacterium belonging to the Rickettsiaceae family inhabits the cytoplasm of the marine ciliate Diophrys appendiculata (Ciliophora, Hypotrichia). Microb Ecol. 2005; 49(3):434-42. DOI: 10.1007/s00248-004-0055-1. View

13.

Sabaneyeva E, Fokin S, Gavrilova E, Kornilova E . Nocodazole inhibits macronuclear infection with Holospora obtusa in Paramecium caudatum. Protoplasma. 2005; 226(3-4):147-53. DOI: 10.1007/s00709-005-0121-7. View

14.

Vannini C, Ferrantini F, Schleifer K, Ludwig W, Verni F, Petroni G . "Candidatus anadelfobacter veles" and "Candidatus cyrtobacter comes," two new rickettsiales species hosted by the protist ciliate Euplotes harpa (Ciliophora, Spirotrichea). Appl Environ Microbiol. 2010; 76(12):4047-54. PMC: 2893493. DOI: 10.1128/AEM.03105-09. View

15.

Fellous S, Quillery E, Duncan A, Kaltz O . Parasitic infection reduces dispersal of ciliate host. Biol Lett. 2010; 7(3):327-9. PMC: 3097846. DOI: 10.1098/rsbl.2010.0862. View

16.

Schrallhammer M, Galati S, Altenbuchner J, Schweikert M, Gortz H, Petroni G . Tracing the role of R-bodies in the killer trait: absence of toxicity of R-body producing recombinant E. coli on paramecia. Eur J Protistol. 2012; 48(4):290-6. DOI: 10.1016/j.ejop.2012.01.008. View

17.

Sun H, Noe J, Barber J, Coyne R, Cassidy-Hanley D, Clark T . Endosymbiotic bacteria in the parasitic ciliate Ichthyophthirius multifiliis. Appl Environ Microbiol. 2009; 75(23):7445-52. PMC: 2786411. DOI: 10.1128/AEM.00850-09. View

18.

PREER Jr J, Stark P . Cytological observations on the cytoplasmic factor "kappa" in Paramecium aurelia. Exp Cell Res. 1953; 5(2):478-91. DOI: 10.1016/0014-4827(53)90234-1. View

19.

Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar . ARB: a software environment for sequence data. Nucleic Acids Res. 2004; 32(4):1363-71. PMC: 390282. DOI: 10.1093/nar/gkh293. View

20.

Amann R, Binder B, Olson R, Chisholm S, Devereux R, Stahl D . Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990; 56(6):1919-25. PMC: 184531. DOI: 10.1128/aem.56.6.1919-1925.1990. View