Distribution and physiology of Alphaproteobacteria living in symbiosis with marine gutless oligochaetes

Abstract

Symbioses are ubiquitous on earth and can be found across all kingdoms of life. The term symbiosis describes two organisms of different kind living together in a long-term and intimate association. One specific type are nutritional animal-microbe symbioses in which microorganisms provide metabolic functions and enable their animal hosts to thrive in otherwise inaccessible environments. Gutless oligochaetes from shallow water marine habitats are one example of such symbioses. The annelid worms entirely lost their digestive and excretory organs. Instead, they rely on nutrients and energy provided by a diverse but specific set of subcuticular but extracellular symbionts. Research has mostly focused on their chemosynthetic gammaproteobacterial and the sulfur-reducing deltaproteobacterial symbionts although Alphaproteobacteria have been shown early on to be partners in these symbioses. Alphaproteobacteria are an abundant, diverse and multifunctional class of bacteria and are promising to provide a plethora of functions to the gutless oligochaete symbiosis. However, little research has focused on their role in the gutless oligochaete symbiosis, which remains to be elucidated. This thesis is a first step to characterize the taxonomic and functional diversity of Alphaproteobacteria in marine gutless oligochaetes. In the first part (Chapter I), I give an overview of the Alphaproteobacteria that associate with gutless oligochaetes and provide directions for promising clades for further research. In the second part, I describe two specific, yet distinct symbiont species. One is a globally distributed representative of the common subcuticular symbiont community and is most abundant in Olavius ilvae in the Mediterranean Sea. This Alphaproteobacterium is a heterotroph and thrives on a variety of sugar compounds (Chapter II). The other one is a low abundant symbiont in the intensively studied Olavius algarvensis community. It stands out by its highly reduced genome and represents one of the smallest bacterial genomes described from a marine animal-microbe symbiosis to date (Chapter III). I used metagenomics, -transcriptomics and -proteomics approaches along with fluorescence in situ hybridization to gain insight into the symbiont taxonomy, their metabolic function and integration into the symbiont community, and their location inside the hosts’ body. Overall, my research sheds light on the most diverse class of gutless oligochaete symbionts – the Alphaproteobacteria – and provides the basis for future research on individual exciting symbiont clades.