Development and Symbiosis Establishment in the Cnidarian Endosymbiosis Model Aiptasia sp.

Abstract

Symbiosis between photosynthetic algae and heterotrophic organisms is widespread. One prominent example of high ecological relevance is the endosymbiosis between dinoflagellate algae of the genus Symbiodinium and reef-building corals, which typically acquire symbionts anew each generation during larval stages. The tropical sea anemone Aiptasia sp. is a laboratory model system for this endosymbiosis and, similar to corals, produces non-symbiotic larvae that establish symbiosis by phagocytosing Symbiodinium from the environment into the endoderm. Here we generate the first overview of Aiptasia embryogenesis and larval development and establish in situ hybridization to analyze expression patterns of key early developmental regulators. Next, we quantify morphological changes in developing larvae and find a substantial enlargement of the gastric cavity over time. Symbiont acquisition starts soon after mouth formation and symbionts occupy a major portion of the host cell in which they reside. During the first 14 days of development, infection efficiency remains constant while in contrast, localization of phagocytosed symbionts changes, indicating that the occurrence of functional phagocytosing cells may be developmentally regulated. Taken together, here we provide the essential framework to further develop Aiptasia as a model system for the analysis of symbiosis establishment in cnidarian larvae at the molecular level.

Marine Invertebrate Larvae Associated with Symbiodinium: A Mutualism from the Start?

“…Only recently, a study by Mohamed et al (2016) detected a transient period of differential expression involving a limited number of genes (3% of assayed transcriptome) 4 h after the exposure of Acropora digitifera planula larvae to a competent strain of Symbiodinium. While yet to be applied for larval studies, symbiosis-specific genes have been identified recently in Aiptasia anemones (Bucher et al, 2016;Wolfowicz et al, 2016). From the symbiont perspective, apart from the identification of protein kinases that may be involved in the establishment of symbiosis (Rosic et al, 2014), a symbiosisspecific gene was identified in Symbiodinium clade A, an H + -ATPase (Bertucci et al, 2010).…”

No genome is an island: toward a 21st century agenda for evolution

“…Numerous bacterial endosymbionts inhabit eukaryotic hosts that reproduce in a vegetative fashion, such as fungi, ciliated protozoa, and amoebae (which serve as hosts to a broad range of bacteria that also infect plant and animal cells) . In sexually reproducing hosts where germline cells are not infected, endosymbionts are maintained transgenerationally by repeated episodes of infection or phagocytosis . Both bacteria and archaea can become endosymbionts, although the overwhelming majority of reports involve bacteria .…”

“…39,40 In sexually reproducing hosts where germline cells are not infected, endosymbionts are maintained transgenerationally by repeated episodes of infection or phagocytosis. 41,42 Both bacteria and archaea can become endosymbionts, although the overwhelming majority of reports involve bacteria. 43 Archaeal endosymbionts have been identified in the cells of an anaerobic marine protist, and much remains to be discovered about other archaeal endosymbionts.…”

Dinoflagellate symbionts escape vomocytosis by host cell immune suppression

“…The long-term pairings between cnidarian hosts and eukaryotic dinoflagellate symbionts (family Symbiodinaceae) (LaJeunesse et al, 2018) are evolutionarily ancient and highly specific (Coffroth et al, 2010;Hambleton et al, 2014;LaJeunesse et al, 2004); yet cnidarians also phagocytose inert beads (Bucher et al, 2016), associate transiently with heterologous symbiont strains (Dunn and Weis, 2009;Hambleton et al, 2014;Matthews et al, 2017;Wolfowicz et al, 2016), and with Chromera velia, a chromerid microalga that is closely related to apicomplexan parasites (Cumbo et al, 2013;Mohamed et al, 2018). Unlike true symbionts, however, these non-symbiotic microalgae fail to engage in lasting relationships with their host.…”

“…To gain insight into the mechanisms that support intracellular maintenance of symbionts and removal of non-symbiotic microorganisms, we exploited the ability of naturally aposymbiotic (symbiont-free) Aiptasia larvae to phagocytose symbionts from the environment (Bucher et al, 2016;Hambleton et al, 2014;Wolfowicz et al, 2016). We screened seven distinct microalgae from four phyla ( Fig.…”