Abstract
The ability of symbionts to recolonize their hosts after a period of dysbiosis is essential to maintain a resilient partnership. Many cnidarians rely on photosynthate provided from a large algal symbiont population. Under periods of thermal stress, symbiont densities in host cnidarians decline, and the recovery of hosts is dependent on the re-establishment of symbiosis. The cellular mechanisms that govern this process of colonization are not well-defined and require further exploration. To study this process in the symbiotic sea anemone model Exaiptasia diaphana, commonly called Aiptasia, we developed a non-invasive, efficient method of imaging that uses autofluorescence to measure the abundance of symbiont cells, which were spatially distributed into distinct cell clusters within the gastrodermis of host tentacles. We estimated cell cluster sizes to measure the occurrence of singlets, doublets, and so on up to much larger cell clusters, and characterized colonization patterns by native and non-native symbionts. Native symbiont Breviolum minutum rapidly recolonized hosts and rapidly exited under elevated temperature, with increased bleaching susceptibility for larger symbiont clusters. In contrast, populations of non-native symbionts Symbiodinium microadriaticum and Durusdinium trenchii persisted at low levels under elevated temperature. To identify mechanisms driving colonization patterns, we simulated symbiont population changes through time and determined that migration was necessary to create observed patterns (i.e., egression of symbionts from larger clusters to establish new clusters). Our results support a mechanism where symbionts repopulate hosts in a predictable cluster pattern, and provide novel evidence that colonization requires both localized proliferation and continuous migration.
Highlights
The ecological success of many cnidarian species relies on their nutritional symbiosis with endosymbiotic dinoflagellate algae to provide nutrient-rich photosynthate in nutrient-poor environments (Muscatine and Porter, 1977)
We find that migratory events after initial inoculation play a critical role throughout symbiont colonization, and that thermal stress impacts symbiont density on a localized scale in a speciesspecific manner
Experimental Aiptasia polyps were generated from animal stocks of the clonal H2 strain containing their native symbiont species B. minutum, originally isolated from a single individual collected from Coconut Island, Kaneohe, Hawaii (Xiang et al, 2013)
Summary
The ecological success of many cnidarian species relies on their nutritional symbiosis with endosymbiotic dinoflagellate algae (family Symbiodiniaceae; LaJeunesse et al, 2018) to provide nutrient-rich photosynthate in nutrient-poor environments (Muscatine and Porter, 1977). These photosynthetic algae reside in vesicles called symbiosomes inside gastrodermal cells of the host cnidarian (Fitt and Trench, 1983; Wakefield et al, 2000). Once ingested into the cnidarian gastrovascular cavity, algal symbionts colonize the cnidarian gastrodermis via host cell phagocytic pathways (Colley and Trench, 1983; Davy et al, 2012). Symbiont populations increase to populate the entire host gastrodermis This intracellular relationship is vulnerable to environmental stress throughout the life history of the host. As environmental changes occur more rapidly worldwide, the mechanisms governing these host-symbiont dynamics and the ability to recover from dysbiosis has become consequential for the fate of coral reef ecosystems across the planet
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