What choanoflagellates can teach us about symbiosis

Abstract

Environmental bacteria influence many facets of choanoflagellate biology, yet surprisingly few examples of symbioses exist. We need to find out why, as choanoflagellates can help us to understand how symbiosis may have shaped the early evolution of animals.

Fig 1. Choanoflagellate–bacteria interactions.

(A) Choanoflagellates survive by eating bacteria. Schematic of a feeding choanoflagellate cell highlighting their “collar complex”: the apical flagellum surrounded by an actin-filled microvilli collar (A). Flagellar beating draws bacterial prey (blue) into the collar, where they become trapped and phagocytosed at the collar membrane. Bacteria are later digested in food vacuoles. n = nucleus. DIC image of Salpingoeca rosetta consuming environmental bacteria (A′). Scale bar = 5 μm. (B) Bacterial cues regulate S. rosetta developmental transitions. Specific cues produced by environmental bacteria regulate rosette development and sexual reproduction. Lipid cofactors produced by Algoriphagus machipongonensis act synergistically to regulate multicellular rosette development in unicellular swimmer cells. A chondroitin lyase produced by Allivibrio fischeri induces swimmer cells to mate and undergo sexual reproduction. Other S. rosetta developmental transitions are influenced by nutrient availability (*), and we hypothesize that these might also be regulated by bacteria. (C) Common bacterially produced metabolites induce collective cell contractions in Choanoeca flexa. Cell contractions that result in colony inversion can be triggered either by exogenous nitric oxide (NO) or by light-to-dark transitions in the presence of retinal produced by environmental bacteria. (D) Barroeca monosierra forms stable, physical associations with bacteria (D). Maximum intensity projection of an immunostained B. monosierra colony shows that the hollow center is filled with bacterial DNA, revealed by Hoechst staining (D′). Apical flagella are highlighted in white, microvilli are highlighted in red, and nuclei are highlighted in cyan. Thin section through an S. monosierra colony, imaged by transmission electron microscopy, reveals the presence of bacteria in the central cavity (D′′). Figure adapted from [11]. Scale bars = 5 μm. (E) Choanoeca sp. produce tubes of extracellular matrix that are stably colonized by bacteria (E). DIC imaging of a single Choanoeca sp. colony at 2 different Z positions shows bacteria colonizing the interior (E′) and surface (E′′) of tubed projections. Scale bars = 20 μm.