Mating in the Closest Living Relatives of Animals Is Induced by a Bacterial Chondroitinase

Abstract

Summary We serendipitously discovered that the marine bacterium Vibrio fischeri induces sexual reproduction in one of the closest living relatives of animals, the choanoflagellate Salpingoeca rosetta. Although bacteria influence everything from nutrition and metabolism to cell biology and development in eukaryotes, bacterial regulation of eukaryotic mating was unexpected. Here we show that a single V. fischeri protein, the previously uncharacterized EroS, fully recapitulates the aphrodisiac-like activity of live V. fischeri. EroS is a chondroitin lyase; although its substrate, chondroitin sulfate, was previously thought to be an animal synapomorphy, we demonstrate that S. rosetta produces chondroitin sulfate and thus extend the ancestry of this important glycosaminoglycan to the premetazoan era. Finally, we show that V. fischeri, purified EroS, and other bacterial chondroitin lyases induce S. rosetta mating at environmentally-relevant concentrations, suggesting that bacteria likely regulate choanoflagellate mating in nature.

Lessons from simple marine models on the bacterial regulation of eukaryotic development

“…Only under starvation conditions would a small fraction of the S. rosetta population mate [21]. A serendipitous observation revealed that specific environmental bacteria, missing from most laboratory cultures, were capable of triggering a population-wide switch to sexual reproduction [22 •• ]. …”

“…Genetic experiments confirmed that the diploid products of cell and nuclear fusion later generated meiotic progeny, demonstrating that V. fischeri bacteria induce the full sexual cycle in S. rosetta (Figure 1b). We subsequently found that Vibrio orientalis and Vibrio tubiashii elicit swarming and mating in S. rosetta , while other species tested did not, suggesting that S. rosetta mating in nature might be regulated by some, but not all species of Vibrio bacteria [22 •• ]. …”

“…Not only does EroS trigger mating at picomolar concentrations, but S. rosetta swarms in response to as few as 400 V. fischeri cells/mL — a density similar to that of V. fischeri in oligotrophic oceans [25]. In addition to V. fischeri , other species of Vibrio bacteria also induce mating in S. rosetta (including V. orientalis and V. tubiashii ), as do commercial chondroitin lyases isolated from Flavobacterium heparinum and Proteus vulgaris [22 •• ], suggesting that encounters between S. rosetta and molecules produced by mating-inducing bacteria might be common occurrences in the ocean.…”

Functions of the Microbiota for the Physiology of Animal Metaorganisms

“…An additional example from S. rosetta suggests that bacteria regulate eukaryotic sexual reproduction. Vibrio fischeri secretes chondroitin lyase, which in S. rosetta initiates the switch from asexual to sexual reproduction by inducing swarming [61]. …”

EroS Enzyme from Aliivibrio fischeri Plays Cupid to Choanoflagellates

“…[11] While this organism is known to form its namesake rosette colonies by (asexual) cell division, the authors clearly noticed different cells swarming together. Upon closer inspection, the authors also observed that within this clump, the organisms began to pair off and reproduce sexually (Figure 2), observing nuclear combination to form a diploid parent.…”