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The Moorena bouillonii and Alpheus frontalis Symbiosis: Patterns in Chemical Ecology, Chemogeography, and Genomics

Abstract

The tropical marine benthic filamentous cyanobacterium Moorena bouillonii and the snapping shrimp Alpheus frontalis engage in a charismatic symbiosis, in which the shrimp weaves the cyanobacterial filaments into tubes and hollow chambers in and around coral reefs. Pairs of A. frontalis live in and feed upon these M. bouillonii structures. M. bouillonii produces a vast arsenal of biologically active and structurally diverse natural products, suggesting that A. frontalis may benefit from an associational defense. It is unclear, however, how M. bouillonii may benefit from this partnership, and what impact the symbiosis may have on the surrounding reef. Also unknown is what role chemistry plays in directing the interactions between the shrimp and cyanobacterium. Furthermore, the breadth of chemodiversity currently known from M. bouillonii that originates from a small collection of discrete locations, paired with the broad distribution of the M. bouillonii – A. frontalis symbiosis across the Indian Ocean and the western tropical Pacific raises the question of what more chemical diversity there is to be discovered in relation to this association. Field surveys and photographic documentation were employed to better understand how M. bouillonii – A. frontalis colonies are distributed across scleractinian coral reefs in the Mariana Islands, and revealed that colonies tend to inhabit interstices in the reef. Nutrient analysis of paired water samples and culturing experiments suggested that A. frontalis may benefit M. bouillonii via an enriched nutrient environment. Competing hypotheses on why shrimp are found in association with certain chemotypes of the cyanobacterium propelled a series of behavioral assays and comparative gas chromatography – mass spectrometry experiments to ultimately yield a lead compound for a shrimp attractant waterborne chemical cue produced by M. bouillonii. Chemogeographic investigations utilizing liquid chromatography – tandem mass spectrometry facilitated the discovery of a regionally specific family of natural products, while also improving understanding of how M. bouillonii chemodiversity is distributed across geographic space and generating paths forward for future discovery. Development of a new bioinformatic tool provided substantial improvements to M. bouillonii genome contiguity, allowing for new insights into the concentrations of potential biosynthetic diversity across compound classes.

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