Abstract
Bacterially-produced small molecules exert profound influences on animal health, morphogenesis, and evolution through poorly understood mechanisms. In one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta, we find that rosette colony development is induced by the prey bacterium Algoriphagus machipongonensis and its close relatives in the Bacteroidetes phylum. Here we show that a rosette inducing factor (RIF-1) produced by A. machipongonensis belongs to the small class of sulfonolipids, obscure relatives of the better known sphingolipids that play important roles in signal transmission in plants, animals, and fungi. RIF-1 has extraordinary potency (femtomolar, or 10(-15) M) and S. rosetta can respond to it over a broad dynamic range-nine orders of magnitude. This study provides a prototypical example of bacterial sulfonolipids triggering eukaryotic morphogenesis and suggests molecular mechanisms through which bacteria may have contributed to the evolution of animals.DOI:http://dx.doi.org/10.7554/eLife.00013.001.
Highlights
Eukaryotes evolved in a world filled with bacteria and throughout their shared history these two branches of life have developed a complex set of ways to compete and cooperate with each other
In the choanoflagellate Salpingoeca rosetta, rosette-shaped multicellular colonies develop when a single founder cell undergoes multiple rounds of incomplete cytokinesis, leaving neighboring cells physically attached by fine intercellular bridges (Fairclough et al 2010; Dayel et al 2011)
Bacteria are most familiar as pathogens, some bacteria produce small molecules that are essential for the biology of animals and other eukaryotes, the details of the ways in which these bacterial molecules are beneficial are not well understood
Summary
Eukaryotes evolved in a world filled with bacteria and throughout their shared history these two branches of life have developed a complex set of ways to compete and cooperate with each other. While research on these interactions has historically emphasized bacterial pathogens, bacteria regulate the biology of eukaryotes in many other ways (McFall-Ngai 1999; Koropatnick et al 2004; Mazmanian et al 2005; Falkow 2006; Hughes and Sperandio 2008; Desbrosses and Stougaard 2011) and may have exerted critical influences on animal evolution. Some choanoflagellates have both solitary and multicellular stages in their life histories (Leadbeater 1983; Karpov and Coupe 1998; Dayel et al 2011) and understanding the environmental cues that regulate choanoflagellate colony formation could provide a molecular model for animal multicellularity
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