Enzyme donation by widespread Rickettsiales in protists and simple aquatic invertebrates

Rickettsiales are intracellular bacteria that depend on their eukaryotic hosts" resources for their metabolism. One clade of aquatic Rickettsiales of the family Midichloriaceae is among the most ubiquitous bacterial phylotypes in aquatic samples, occurring in almost 10% of all aquatic samples. With a large host diversity of protists and early branching animals such as sponges, placozoans, and cnidarians, these Midichloriaceae are regarded mainly as parasites or pathogens and were linked to coral disease outbreaks.

Here, I will present evidence for a surprising and highly beneficial role for these intracellular symbionts that inhabit the endoplasmic reticulum in most of their hosts - digestive enzyme donation. Across all host groups, data from genomic, expression, enzyme characterization, and imaging experiments show that these ubiquitous aquatic Midichloriaceae provide enzymes to break down sugar-based macromolecules. Based on the characterization of heterologously expressed enzymes, the symbionts provide digestive enzymes for laminarin, one of the most abundant macromolecules in aquatic systems. In addition, our data show an anti-microbial role, as one broadly-expressed enzyme can attack the cell walls of bacteria. Using in-depth tree-reconciliation analyses, I will discuss the evolutionary chains of events that likely led to the taming of notorious parasites into important intracellular symbionts that can turn dietary fibers into efficient metabolic resources for sugars. These insights into the beneficial roles of a group of symbionts labeled parasitic because of their intracellular lifestyle will provide a better understanding of these common symbioses that can alter physiology, ecology, and gene flow from within host cells. Given their broad host range and geographic distribution, these aquatic Midichloriaceae are at the center of many current frontiers of aquatic sciences on a changing planet, such as biomonitoring and conservation efforts, aquaculture, and the aquarium trade.