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The microbiome of a colonial choanoflagellate from Mono Lake, CA


Animals first evolved in a world inhabited by bacteria, and early animal-bacterial interactions may have shaped animal evolution. Understanding these ancient interactions could elucidate fundamental rules that govern modern-day animal-bacterial relationships. Bacteria affect many aspects of animal biology, from being a food source for sponges, metabolizing complex molecules in the termite gut, shaping immune system development in vertebrates, and driving light organ morphogenesis in the bobtail squid. Animals are multicellular organisms with a diverse array of cell types that can associate with complex bacterial communities, leading to an inherent challenge in teasing apart the molecular mechanisms underlying these interactions. Experimentally tractable model systems are essential for studying host-bacterial interactions because they provide the opportunity to uncover mechanisms that may be conserved in the animal kingdom.

Choanoflagellates are aquatic microeukaryotes and the closest living relatives of animals. Due to their phylogenetic placement, they provide a unique opportunity to investigate biological phenomena that might be conserved with animals or that were present in their last common ancestor with animals. Choanoflagellates interact with bacteria in a diversity of ways. Their primary interaction is to phagocytose bacteria as their food source. The model choanoflagellate, Salpingoeca rosetta, can also respond to an array of bacterial cues resulting in the developmental of multicellular colonies from single cells or a swarming behavior followed by mating. My doctoral research focuses on a new choanoflagellate species, Salpingoeca monosierra, that harbors the first stable microbiome observed in a choanoflagellate (Chapter 2).

S. monosierra was isolated from Mono Lake (alkaline soda lake; pH 10, salinity 8.1%) and forms large spherical colonies (up to 125 µm diameter) that are more than an order of magnitude larger than those formed by S. rosetta. Live-cell imaging, TEM, and fluorescent in situ hybridization revealed that S. monosierra colonies are filled with both an extracellular matrix and bacterial symbionts from four different bacterial families: Saccharospirillaceae, Oceanospirillaceae, Ectothiorhodospiraceae, and Rhodobacteraceae. Close relatives of the symbionts are known symbionts of many marine invertebrates and other prokaryotes. Treatment of the S. monosierra colonies with antibiotics reduced bacterial load inside the colonies and ultimately colony size, suggesting that bacteria may be influencing colony size. We found two main similarities between S. monosierra microbiome and the animal gut microbiome. First, the observation of bacterial cells between choanoflagellate cells is reminiscent of invading pathogenic bacteria. Second, the arrangement of the epithelial-like choanoflagellate cells surrounding the glycoprotein rich extracellular matrix and bacteria is reminiscent of the animal gut epithelium encompassing the mucus barrier and gut microbiota. This tractable model system holds the potential to unlock mechanisms underlying one of the most complex animal-bacterial interactions, the animal gut microbiome.

Choanoflagellates are also a promising model for investigating other aspects of animal cell biology, including cell-cell signaling. Tyrosine kinase (TK) signaling is a hallmark of animal intercellular signaling that operates as a dynamic molecular switch initiating signaling cascades in development, differentiation, proliferation, and homeostasis. Choanoflagellate genomes reveal the presence of a comparable number of tyrosine kinases and accompanying signaling components as those found in animals. I sought to explore the role of TK signaling in choanoflagellate multicellular development and if it is functioning in a way that is comparable to TK signaling in animals (Appendix). We found tyrosine phosphorylated proteins enriched at the basal poles of every cell in a colony, reminiscent of the animal epithelia. This localization was also found in S. monosierra. Although few differences were identified between single cells and rosettes in the tyrosine phospho-proteome by immunoblot analysis, further investigation of the role of tyrosine kinase signaling in colony development may provide insight into how TK signaling contributed to the evolution of animal multicellularity and how complex signaling networks arose.

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