Population‐level dynamics in experimental mixed infections: evidence for competitive exclusion among bacterial parasites of Paramecium caudatum

Abstract

Parasites frequently share their host populations with other parasites. However, little is known about how different parasites respond to competition with diverse competitor species in the within‐host and between‐host environments. We explored the repeatability of competition by simultaneously exposing microcosm populations of the ciliate Paramecium caudatum to pairs of parasites from the Holospora species complex (H. undulata, H. caryophila and H. obtusa). We measured how competition affected the persistence and prevalence of each compared to single infections, across three host genotypes. Three weeks post‐inoculation we identified the presence of each parasite using fluorescence in situ hybridisation (FISH). Competitive exclusion (62/72) was more common than co‐existence (10/72) in populations inoculated with two parasites. There was a clear pattern of competitive superiority, with H. caryophila persisting in all doubly inoculated populations (with either H. undulata or H. obtusa), and H. undulata tending to exclude H. obtusa. This mirrored infection success in single infections, with H. caryophila having a higher infection prevalence in single inoculations, followed by H. undulata then H. obtusa. The probability of persistence in co‐inoculations did not change across the different host genotypes, and prevalence was the same as in single infections. Our results are consistent with superinfection models, which assume the competitive exclusion of parasites upon contact within the same host. Furthermore, such non‐random competitive epidemiological dynamics, where one parasite always wins, may be of interest for public health management, especially if the winning parasite is avirulent, as is seemingly the case here.

Among-Strain Variation in Resistance of Paramecium caudatum to the Endonuclear Parasite Holospora undulata: Geographic and Lineage-Specific Patterns

“…Following the discovery of Holospora bacteria in the 19th century ( Hafkine, 1890 ), there has been extensive research on their morphology, infection life cycle, and taxonomic relationships [for a historical overview, see Fokin and Görtz (2009) ]. More recently, the Paramecium-Holospora system has served as a model to study epidemiology and evolution in experimental microcosms ( Lohse et al, 2006 ; Nidelet et al, 2009 ; Duncan et al, 2011a , 2015 , 2018 ; Castelli et al, 2015 ; Dusi et al, 2015 ; Nørgaard et al, 2020 ; Zilio et al, 2020a , b ).…”

Social immunity modulates competition between coinfecting pathogens

“…How successful a pathogen is in infecting the host and producing transmission stages will thus strongly depend on the presence and type of coinfecting pathogens in the host, and whether and how the host interacts with conspecifics. Recent theoretical and experimental research has made significant progress in understanding, on the one hand, some of the consequences of coinfections on virulence and pathogen epidemiology in individual hosts (Thomas et al ; de Roode et al ; Choisy & de Roode ; Cressler et al ; Susi et al ; Ramiro et al ; Duncan et al ); and on the other, how social immunity interferes with the course of infection in individual hosts and pathogen spread through the colony (Stroeymeyt et al ; Pull et al ). However, how the social interactions between hosts could affect pathogen competition in infected individuals and how this may affect the overall pathogen community is largely unexplored.…”

The Obligate Symbiont “Candidatus Megaira polyxenophila” Has Variable Effects on the Growth of Different Host Species

“…This ciliate is studied, among other things ( Karunanithi et al, 2019 ; Kelz and Mashour, 2019 ; Mayne et al, 2019 ; Soares et al, 2019 ; Arnaiz et al, 2020 ) for the abundance and diversity of its endosymbionts ( Floriano et al, 2018 ; Garushyants et al, 2018 ; Grosser et al, 2018 ; Potekhin et al, 2018 ; Sabaneyeva et al, 2018 ; Schrallhammer et al, 2018 ; Castelli et al, 2019a , b ; Fokin et al, 2019 ; Koehler et al, 2019 ; Lanzoni et al, 2019 ; Plotnikov et al, 2019 ). Host-symbiont interactions and their outcome have been studied for example using Holospora ( Lohse et al, 2006 ; Hori et al, 2008 ; Fokin and Görtz, 2009 ; Nidelet et al, 2009 ; Duncan et al, 2013 , 2018 ; Banerji et al, 2015 ; Castelli et al, 2015 ; Dusi et al, 2015 ; Garushyants et al, 2018 ; Grosser et al, 2018 ) Caedibacter ( Kusch et al, 2002 ; Dusi et al, 2014 ; Grosser et al, 2018 ; Schu and Schrallhammer, 2018 ; Koehler et al, 2019 ) and Preeria ( Bella et al, 2016 ; Potekhin et al, 2018 ). Despite an increasing number of studies, our knowledge about the impact of symbionts on Paramecium is limited, especially when considering that this ciliate is among the best studied protists in regard to host-symbiont interactions.…”