Towards functional ecology of environmental chlamydiae

Chlamydiae are bacteria commonly known as serious pathogens of humans and animals, causing over a hundred million infections worldwide each year. It is less well known that closely related bacteria have also been discovered in the environment, where they live primarily as symbionts within unicellular eukaryotes (protists). Like their pathogenic counterparts, these environmental chlamydiae rely largely on nutrients and other compounds from their eukaryotic hosts and thus cannot survive on their own. Their analysis has revealed novel and fascinating insights into the evolution of the unique chlamydial lifestyle and the emergence of efficient mechanisms to infect eukaryotes, including humans, animals, and protists. However, our understanding of chlamydiae is so far based on only few strains that have been studied under controlled laboratory conditions. Inspired by recent evidence that chlamydiae are rare yet ubiquitous members in diverse environments worldwide, this project aims at characterizing natural chlamydial communities and their impact through food webs on microbes and higher eukaryotic organisms. Using state-of-the-art molecular and analytic methods (such as targeted amplicon sequencing, single cell genomics, and isotope probing assays) we will for the first time be able to characterize chlamydial community composition and dynamics in nature, and reveal their effect on elemental cycles in diverse environments. Employingsophisticated isolation approaches, we will recover and characterize representatives of yet uncharacterized environmental chlamydiae, providing a broad and comprehensive perspective on the diversity of this unique group of host-associated microbes. It is only recently that we began to realize the importance of intimate relationships with microbes, essentially for all living beings on our planet. The chlamydiae can serve as a model and blueprint to study the evolution of these associations and molecular mechanisms mediating microbe-host interaction.

This project aimed to deepen our understanding of the diversity, ecology, and evolution of the bacterial phylum Chlamydiota. These obligate intracellular bacteria include major human and animal pathogens like Chlamydia trachomatis, as well as a broad diversity of chlamydiae that live as symbionts of protists found everywhere on planet Earth. As chlamydiae are ancient and all known members of the phylum are obligate intracellular microorganisms, they serve as ideal model to study the evolution of symbiosis and microbe host interaction. Using a comprehensive dataset of chlamydial genome sequences generated by us and others, we reconstructed the genetic repertoire of the last common chlamydial ancestor, which had an unexpected anoxic and motile, yet intracellular lifestyle, and contained a plasmid facilitating the exchange of genetic material. Contrary to the genome reduction processes seen in other intracellular bacteria, we found that genome evolution of chlamydiae thriving as endosymbionts of protists was characterized by genome expansion through gene acquisition, which enhanced their metabolic potential and adaptability to various environmental conditions their hosts face. Members of other chlamydial lineages adapted to narrower host ranges, showing signs of current genome reduction. By comparing genomes from different chlamydial lineages, we showed that chlamydiae are much more versatile than previously thought, but that the core genes shared by all chlamydiae are sufficient to infect a wide range of hosts from protists to corals and arthropods. The ability to infect chordate and mammalian hosts though seems to be restricted to a few chlamydial lineages and to depend on the stepwise acquisition and adaptation of genes to cope with the adaptive immune response and cell differentiation. Additionally, we confirmed the presence of chlamydiae inside coral tissue through microscopy and genome analysis and cultivated the first chlamydiae infecting autotrophic host organisms, unicellular dinoflagellates, which themselves thrive as symbionts of corals. Both findings have potential implications for coral reef health and management, which are crucial for marine ecosystems. Besides marine ecosystems, we demonstrated that chlamydiae are rare but diverse and stable members of sediments and soils. Importantly, we showed that as symbionts of protists, though so far neglected, chlamydiae impact ecosystems by affecting their hosts. In summary, we increased knowledge about the evolution of intracellular chlamydial symbionts and pathogens and highlighted the role of protist symbionts in ecosystems.