Chiriac, M.-C. | Search bioRxiv

bioRxiv2023

Rickettsiales' deep evolutionary history sheds light on the emergence of intracellular lifestyles

Ancient bacteria largely lived and flourished as free-living cells till the rise of eukaryotes triggered their adaptation to a new habitat: the intracellular milieu. Rickettsiales bacteria are the most prevalent intracellular microorganisms discovered and the culprits behind some of mankinds worst pestilential diseases. Here, we show that intracellularity is not a defining feature of the group and describe the eco-evolutionary processes that transformed harmless free-living bacteria into obligate intracellular symbionts and parasites. We found that the evolution of free-living lineages towards enhanced cross-feeding interactions with microbial eukaryotes trapped them in a nutritional bind to their trophic partners. We discovered that the oldest Rickettsiales lineages are the closest relatives to modern eukaryotes and are enriched in proteins predicted to have been present in the mitochondrial ancestor. This study not only opens avenues for the detection and surveillance of emerging diseases but also expands our understanding of the origins of complex life. One-Sentence SummaryCross-feeding interactions shaped Rickettsiales genomic architectures along the parasite/free-living spectrum

microbiology↗

bioRxiv2021

Heliorhodopsin evolution is driven by photosensory promiscuity in monoderms

The ability to harness Suns electromagnetic radiation by channeling it into high-energy phosphate bonds empowered microorganisms to tap into a cheap and inexhaustible source of energy. Lifes billion-years history of metabolic innovations led to the emergence of only two biological complexes capable of harvesting light: one based on rhodopsins and the other on (bacterio)chlorophyll. Rhodopsins encompass the most diverse and abundant photoactive proteins on Earth and were until recently canonically split between type-1 (microbial rhodopsins) and type-2 (animal rhodopsins) families. Unexpectedly, the long-lived type-1/type-2 dichotomy was recently amended through the discovery of heliorhodopsins (HeRs) (Pushkarev et al. 2018), a novel and exotic family of rhodopsins (i.e. type-3) that evaded recognition in our current homology-driven scrutiny of lifes genomic milieu. Here, we bring to resolution the debated monoderm/diderm occurrence patterns by conclusively showing that HeR distribution is restricted to monoderms. Furthermore, through investigating protein domain fusions, contextual genomic information, and gene co-expression data we show that HeRs likely function as generalised light-dependent switches involved in the mitigation of light-induced oxidative stress and metabolic circuitry regulation. We reason that HeRs ability to function as sensory rhodopsins is corroborated by their photocycle dynamics (Pushkarev et al. 2018) and that their presence and function in monoderms is likely connected to the increased sensitivity to light-induced damage of these organisms (Maclean et al. 2009).

microbiology↗