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 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. Here, we report the isolation of a social amoeba, Dictyostelium giganteum, naturally infected with a chlamydial symbiont. The social life cycle of dictyostelids is characterized by multicellular stages through aggregation of vegetative trophozoites, leading to the development of multicellular fruiting bodies and the formation of spores. Although dictyostelids undergo symbioses with various bacteria, chlamydiae have only recently been found to be associated with these amoebae. The chlamydial symbiont identified here represents a novel species, Reclusachlamydia socialis, and is retained in all stages of the host's social life cycle. Notably, the symbiont lacks a detectable extracellular form. Combining fluorescence microscopy and quantitative PCR, we show 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 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 host multicellularity.