Epidemiology of Nucleus-Dwelling Holospora: Infection, Transmission, Adaptation, and Interaction with Paramecium

Overview

Journal Results Probl Cell Differ

Specialty Cell Biology

Date 2020 Dec 2

PMID 33263870

Citations 6

Authors

Martina Schrallhammer

Alexey Potekhin

Affiliations

Soon will be listed here.

Abstract

The chapter describes the exceptional symbiotic associations formed between the ciliate Paramecium and Holospora, highly infectious bacteria residing in the host nuclei. Holospora and Holospora-like bacteria (Alphaproteobacteria) are characterized by their ability for vertical and horizontal transmission in host populations, a complex biphasic life cycle, and pronounced preference for host species and colonized cell compartment. These bacteria are obligate intracellular parasites; thus, their metabolic repertoire is dramatically reduced. Nevertheless, they perform complex interactions with the host ciliate. We review ongoing efforts to unravel the molecular adaptations of these bacteria to their unusual lifestyle and the host's employment in the symbiosis. Furthermore, we summarize current knowledge on the genetic and genomic background of Paramecium-Holospora symbiosis and provide insights into the ecological and evolutionary consequences of this interaction. The diversity and occurrence of symbioses between ciliates and Holospora-like bacteria in nature is discussed in connection with transmission modes of symbionts, host specificity and compatibility of the partners. We aim to summarize 50 years of research devoted to these symbiotic systems and conclude trying to predict some perspectives for further studies.

Citing Articles

An Evolutionary-Focused Review of the Holosporales (Alphaproteobacteria): Diversity, Host Interactions, and Taxonomic Re-ranking as Holosporineae Subord. Nov.

Castelli M, Petroni G Microb Ecol. 2025; 88(1):15.

PMID: 40085262 DOI: 10.1007/s00248-025-02509-0.

Hepatincolaceae (Alphaproteobacteria) are Distinct From Holosporales and Independently Evolved to Associate With Ecdysozoa.

Castelli M, Gammuto L, Podushkina D, Vecchi M, Altiero T, Clementi E Environ Microbiol. 2025; 27(1):e70028.

PMID: 39797518 PMC: 11724238. DOI: 10.1111/1462-2920.70028.

Symbionts of Ciliates and Ciliates as Symbionts.

Dagar J, Maurya S, Antil S, Abraham J, Somasundaram S, Lal R Indian J Microbiol. 2024; 64(2):304-317.

PMID: 39010998 PMC: 11246404. DOI: 10.1007/s12088-024-01203-y.

Cellular interactions and evolutionary origins of endosymbiotic relationships with ciliates.

Song Q, Zhao F, Hou L, Miao M ISME J. 2024; 18(1).

PMID: 38916437 PMC: 11253213. DOI: 10.1093/ismejo/wrae117.

"Candidatus Intestinibacterium parameciiphilum"-member of the "Candidatus Paracaedibacteraceae" family (Alphaproteobacteria, Holosporales) inhabiting the ciliated protist Paramecium.

Lanzoni O, Szokoli F, Schrallhammer M, Sabaneyeva E, Krenek S, Doak T Int Microbiol. 2023; 27(3):659-671.

PMID: 37615902 PMC: 11144129. DOI: 10.1007/s10123-023-00414-5.

References

Abamo F, Dohra H, Fujishima M . Fate of the 63-kDa periplasmic protein of the infectious form of the endonuclear symbiotic bacterium Holospora obtusa during the infection process. FEMS Microbiol Lett. 2008; 280(1):21-7. DOI: 10.1111/j.1574-6968.2007.01023.x. View

Boscaro V, Fokin S, 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. 2012; 65(1):255-67. DOI: 10.1007/s00248-012-0110-2. View

Castelli M, Lanzoni O, Rossi L, Potekhin A, Schrallhammer M, Petroni G . Evaluation of Enrichment Protocols for Bacterial Endosymbionts of Ciliates by Real-Time PCR. Curr Microbiol. 2016; 72(6):723-32. DOI: 10.1007/s00284-016-1006-z. View

Castelli M, Sabaneyeva E, Lanzoni O, Lebedeva N, Floriano A, Gaiarsa S . Deianiraea, an extracellular bacterium associated with the ciliate Paramecium, suggests an alternative scenario for the evolution of Rickettsiales. ISME J. 2019; 13(9):2280-2294. PMC: 6776064. DOI: 10.1038/s41396-019-0433-9. View

Cui P, Dong Y, Li Z, Zhang Y, Zhang S . Identification and functional characterization of an uncharacterized antimicrobial peptide from a ciliate Paramecium caudatum. Dev Comp Immunol. 2016; 60:53-65. DOI: 10.1016/j.dci.2016.02.016. View

Dohra H, Tanaka K, Suzuki T, Fujishima M, Suzuki H . Draft genome sequences of three Holospora species (Holospora obtusa, Holospora undulata, and Holospora elegans), endonuclear symbiotic bacteria of the ciliate Paramecium caudatum. FEMS Microbiol Lett. 2014; 359(1):16-8. DOI: 10.1111/1574-6968.12577. View

Duncan A, Fellous S, Accot R, Alart M, Sobandi K, Cosiaux A . Parasite-mediated protection against osmotic stress for Paramecium caudatum infected by Holospora undulata is host genotype specific. FEMS Microbiol Ecol. 2010; 74(2):353-60. DOI: 10.1111/j.1574-6941.2010.00952.x. View

Duncan A, Gonzalez A, Kaltz O . Stochastic environmental fluctuations drive epidemiology in experimental host-parasite metapopulations. Proc Biol Sci. 2013; 280(1769):20131747. PMC: 3768316. DOI: 10.1098/rspb.2013.1747. View

Edgcomb V . Marine protist associations and environmental impacts across trophic levels in the twilight zone and below. Curr Opin Microbiol. 2016; 31:169-175. DOI: 10.1016/j.mib.2016.04.001. View

10.

Eschbach E, Pfannkuchen M, Schweikert M, Drutschmann D, Brummer F, Fokin S . "Candidatus Paraholospora nucleivisitans", an intracellular bacterium in Paramecium sexaurelia shuttles between the cytoplasm and the nucleus of its host. Syst Appl Microbiol. 2009; 32(7):490-500. DOI: 10.1016/j.syapm.2009.07.004. View

11.

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

12.

Fels D, Vignon M, Kaltz O . Ecological and genetic determinants of multiple infection and aggregation in a microbial host-parasite system. Parasitology. 2008; 135(12):1373-83. DOI: 10.1017/S0031182008004940. View

13.

Fujishima M, Kawai M, Yamamoto R . Paramecium caudatum acquires heat-shock resistance in ciliary movement by infection with the endonuclear symbiotic bacterium Holospora obtusa. FEMS Microbiol Lett. 2005; 243(1):101-5. DOI: 10.1016/j.femsle.2004.11.053. View

14.

Fujishima M, Kodama Y . Endosymbionts in paramecium. Eur J Protistol. 2011; 48(2):124-37. DOI: 10.1016/j.ejop.2011.10.002. View

15.

Fujishima M, Nagahara K, Kojima Y, Sayama Y . Sensitivity of the infectious long form of the macronuclear endosymbiont Holospora obtusa of the ciliate Paramecium caudatum against chemical and physical factors. Eur J Protistol. 2012; 27(2):119-26. DOI: 10.1016/S0932-4739(11)80333-0. View

16.

Garushyants S, Beliavskaia A, Malko D, Logacheva M, Rautian M, Gelfand M . Comparative Genomic Analysis of spp., Intranuclear Symbionts of Paramecia. Front Microbiol. 2018; 9:738. PMC: 5911502. DOI: 10.3389/fmicb.2018.00738. View

17.

Gast R, Sanders R, Caron D . Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends Microbiol. 2009; 17(12):563-9. DOI: 10.1016/j.tim.2009.09.001. View

18.

Gillespie J, Kaur S, Rahman M, Rennoll-Bankert K, Sears K, Beier-Sexton M . Secretome of obligate intracellular Rickettsia. FEMS Microbiol Rev. 2014; 39(1):47-80. PMC: 4344940. DOI: 10.1111/1574-6976.12084. View

19.

Gortz H, Fujishima M . Conjugation and meiosis of Paramecium caudatum infected with the micronucleus-specific bacterium Holospora elegans. Eur J Cell Biol. 1983; 32(1):86-91. View

20.

Hori M, Fujii K, Fujishima M . Micronucleus-specific bacterium Holospora elegans irreversibly enhances stress gene expression of the host Paramecium caudatum. J Eukaryot Microbiol. 2009; 55(6):515-21. DOI: 10.1111/j.1550-7408.2008.00352.x. View