Summary
The
R
ickettsiae
comprise intracellular bacterial symbionts and pathogens infecting diverse eukaryotes. Here, we provide a detailed characterization of ‘
C
andidatus
J
idaibacter acanthamoeba’, a rickettsial symbiont of
A
canthamoeba
. The bacterium establishes the infection in its amoeba host within 2 h where it replicates within vacuoles. Higher bacterial loads and accelerated spread of infection at elevated temperatures were observed. The infection had a negative impact on host growth rate, although no increased levels of host cell lysis were seen. Phylogenomic analysis identified this bacterium as member of the
M
idichloriaceae
. Its 2.4 Mb genome represents the largest among
R
ickettsiales
and is characterized by a moderate degree of pseudogenization and a high coding density. We found an unusually large number of genes encoding proteins with eukaryotic‐like domains such as ankyrins, leucine‐rich repeats and tetratricopeptide repeats, which likely function in host interaction. There are a total of three divergent, independently acquired type
IV
secretion systems, and 35 flagellar genes representing the most complete set found in an obligate intracellular
A
lphaproteobacterium
. The deeply branching phylogenetic position of ‘
C
andidatus
J
idaibacter acanthamoeba’ together with its ancient features place it closely to the rickettsial ancestor and helps to better understand the transition from a free‐living to an intracellular lifestyle.