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The choanoflagellate S. rosetta integrates cues from diverse bacteria to enhance multicellular development

  • Author(s): Ireland, Ella
  • Advisor(s): King, Nicole
  • et al.
Abstract

Bacteria play critical roles in regulating animal development, homeostasis and disease. Animals are often hosts to hundreds of different species of bacteria, which produce thousands of different molecules with the potential to influence animal biology. Direct interactions between different species of bacteria, as well as the environmental context of the animal-bacteria interaction, can have a significant impact on the outcome for the animal (Chapter 1). While we are beginning to understand the role of context in bacteria-animal interactions, surprisingly little is known about how animals integrate multiple distinct bacterial inputs.

In my doctoral research I studied the choanoflagellate Salpingoeca rosetta, one of the closest living relatives of animals, to learn more about how eukaryotes integrate diverse bacterial cues. As with animals, bacteria regulate critical aspects of S. rosetta biology. The bacterium Algoriphagus machipongonensis produces sulfonolipid Rosette Inducing Factors (RIFs), which induce multicellular “rosette” development in S. rosetta. In contrast, the bacterium Vibrio fischeri produces a chondroitinase, EroS, which acts as an aphrodisiac and induces S. rosetta to undergo sexual reproduction. Thus, S. rosetta undergoes distinct life history transitions in response to biochemically unrelated bacterial cues. Importantly, both the choanoflagellate and its bacterial partners in these interactions can be independently cultured and manipulated in the lab. This motivated me to use S. rosetta as a simple model for exploring how eukaryotes are influenced by environments filled with diverse bacterial cues.

I investigated how S. rosetta responds to environments containing both the mating inducer EroS and the rosette-inducing RIFs (Chapter 2). I found that the initiation of mating behavior is unchanged in the presence of cues that induce rosette development. In contrast, rosette development is significantly enhanced by the presence of the mating inducer. Simultaneous exposure to RIFs and EroS elicited both larger multicellular colonies and an increase in the number of colonies. These results demonstrate that, rather than conveying conflicting sets of information, these distinct bacterial cues synergize to augment multicellular development. Furthermore, I found that the mating cue EroS induces changes in the extracellular matrix that had previously only been observed during rosette development, suggesting one possible point of intersection for these two pathways (Appendix 1).

These findings highlight how synergistic interactions among bacterial cues can influence the biology of eukaryotes. The model eukaryote S. rosetta integrates cues from diverse bacteria and modulates its response accordingly. Ongoing research investigating the S. rosetta targets of these bacterial cues (Appendix 2) may reveal the mechanistic basis of this synergy. The experimental tractability of S. rosetta and its interactions with bacteria make it an exciting model system in which to investigate the question how eukaryotes sense and respond to diverse bacterial cues.

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