Act together—implications of symbioses in aquatic ciliates

Abstract

Mutual interactions in the form of symbioses can increase the fitness of organisms and provide them with the capacity to occupy new ecological niches. The formation of obligate symbioses allows for rapid evolution of new life forms including multitrophic consortia. Microbes are important components of many known endosymbioses and their short generation times and strong potential for genetic exchange may be important drivers of speciation. Hosts provide endo- and ectosymbionts with stable, nutrient-rich environments, and protection from grazers. This is of particular importance in aquatic ecosystems, which are often highly variable, harsh, and nutrient-deficient habitats. It is therefore not surprising that symbioses are widespread in both marine and freshwater environments. Symbioses in aquatic ciliates are good model systems for exploring symbiont-host interactions. Many ciliate species are globally distributed and have been intensively studied in the context of plastid evolution. Their relatively large cell size offers an ideal habitat for numerous microorganisms with different functional traits including commensalism and parasitism. Phagocytosis facilitates the formation of symbiotic relationships, particularly since some ingested microorganisms can escape the digestion. For example, photoautotrophic algae and methanogens represent endosymbionts that greatly extend the biogeochemical functions of their hosts. Consequently, symbiotic relationships between protists and prokaryotes are widespread and often result in new ecological functions of the symbiotic communities. This enables ciliates to thrive under a wide range of environmental conditions including ultraoligotrophic or anoxic habitats. We summarize the current understanding of this exciting research topic to identify the many areas in which knowledge is lacking and to stimulate future research by providing an overview on new methodologies and by formulating a number of emerging questions in this field.

“Candidatus Sonnebornia yantaiensis”, a member of candidate division OD1, as intracellular bacteria of the ciliated protist Paramecium bursaria (Ciliophora, Oligohymenophorea)

“…These symbiotic associations can increase the fitness of ciliates by endowing the host with the ability to thrive in particular environments, explore new ecological niches, and enhance its defense capabilities against attack or competition [14,25,27]. Studies on the ciliate-symbiont system might provide a clue for a better understanding of the origin and evolution of the eukaryotic cell [24].…”

Molecular and functional ecology of aquatic microbial symbionts

“…Although the ciliate epibionts exhibited high grazing rates on free-living bacteria, their effects on the total bacterial abundance seemed to be rather low. Also, effects of epibionts on the physiology and development of their host require further study.A cluster of three articles (Dziallas et al, 2012; GarciasBonet et al, 2012;McManus et al, 2012) addresses endosymbiotic relationships between microbes and higher organisms. The article by Dziallas et al (2012) reviews knowledge on the diversity, ecological function, and evolution of ciliate symbionts and also points at several future research directions.…”

“…A cluster of three articles (Dziallas et al, 2012; GarciasBonet et al, 2012;McManus et al, 2012) addresses endosymbiotic relationships between microbes and higher organisms. The article by Dziallas et al (2012) reviews knowledge on the diversity, ecological function, and evolution of ciliate symbionts and also points at several future research directions.…”

“…The article by Dziallas et al (2012) reviews knowledge on the diversity, ecological function, and evolution of ciliate symbionts and also points at several future research directions. The article by McManus et al (2012) more specifically addresses chloroplast symbioses in marine ciliates.…”

The symbiotic life ofSymbiodiniumin the open ocean within a new species of calcifying ciliate (Tiarinasp.)

“…Ciliates are also known to acquire phototrophy through photosymbiosis with eukaryotic or prokaryotic microalgal cells (Stoecker et al, 2009;Esteban et al, 2010;Dziallas et al, 2012). In freshwater habitats, many ciliate species (for example, Paramecium bursaria, Coleps hirtus viridis) are found in symbiosis with the green alga Chlorella, whereas in marine ecosystems rare examples of photosymbiosis with eukaryotic microalgae have been reported (Stabell et al, 2002;Stoecker et al, 2009;Johnson, 2011).…”