The adaptation of chlamydiae to facultative host multicellularity

Abstract

The phylum Chlamydiota consists of obligate intracellular bacteria comprising the human pathogen Chlamydia trachomatis and a large variety of species infecting animals and protists. Despite their enormous diversity, a feature shared by all known chlamydiae is their biphasic developmental cycle, consisting of intra- and extracellular stages with substantial differences in morphology and physiology. A similarly remarkable shift occurs in the amoeba Dictyostelium discoideum and related dictyostelids in their so-called social life cycle, leading to the formation of spores through aggregation of vegetative trophozoites and the development of multicellular fruiting bodies. Although dictyostelids undergo symbioses with various bacteria, chlamydiae have only recently been found to be associated with this host. Here we report the isolation of a Dictyostelium giganteum strain naturally infected with a chlamydial symbiont, identified as a novel species, Reclusachlamydia socialis. The symbiont is retained in all stages of the hosts social life cycle and notably lacks an extracellular form. Combining fluorescence microscopy and quantitative PCR we showed that transmission is entirely dependent on cell-to-cell contact during the host aggregation stage. The absence of an extracellular stage is further supported by transmission electron microscopy and the lack of genes essential for chlamydial developmental cycle regulation and extracellular survival. This unprecedented variation of a highly conserved developmental feature that evolved more than a billion years ago illustrates the remarkable adaptability of chlamydiae. This study adds to our understanding of endosymbiosis in the face of facultative multicellularity.