Host Adaptation inLegionellalesIs 1.9 Ga, Coincident with Eukaryogenesis

Abstract

Bacteria adapting to living in a host cell caused the most salient events in the evolution of eukaryotes, namely the seminal fusion with an archaeon, and the emergence of both mitochondrion and chloroplast. A bacterial clade that may hold the key to understanding these events is the deep-branching gammaproteobacterial order Legionellales—containing among others Coxiella and Legionella—of which all known members grow inside eukaryotic cells. Here, by analyzing 35 novel Legionellales genomes mainly acquired through metagenomics, we show that this group is much more diverse than previously thought, and that key host-adaptation events took place very early in its evolution. Crucial virulence factors like the Type IVB secretion (Dot/Icm) system and two shared effector proteins were gained in the last Legionellales common ancestor (LLCA). Many metabolic gene families were lost in LLCA and its immediate descendants, including functions directly and indirectly related to molybdenum metabolism. On the other hand, genome sizes increased in the ancestors of the Legionella genus. We estimate that LLCA lived circa 1.89 Ga ago, probably predating the last eukaryotic common ancestor (LECA) by circa 0.4-1.0 Ga. These elements strongly indicate that host-adaptation arose only once in Legionellales, and that these bacteria were using advanced molecular machinery to exploit and manipulate host cells early in eukaryogenesis.

Host association and intracellularity evolved multiple times independently in theRickettsiales

“…Our reconstruction may also provide a novel perspective on the origin and evolution of other host-associated bacterial lineages that, similarly to Rickettsiales, present the prerogative to "hold the control" of the interaction and to switch hosts by horizontal transmission, and were thus termed "professional symbionts" 61 ) (e.g. Chlamydiae 62 , Legionellales 63 and Holosporales 1 ). These lineages could share similarities in the initial establishment and successive stepwise and "late" evolutionary development.…”

“…Large-scale comparative genomic analyses such as those presented here and elsewhere 10,62,63 have huge potential to provide major advances in our understanding of functional traits and the underlying evolutionary processes. However, they also face inherent predictive limits, being quite suitable for deriving metabolic dependencies, and less for the inference of more complex and possibly not-yet-documented traits, such as mechanisms of interaction and subcellular (or extracellular) localisation.…”

Intrabacterial regulation of a cytotoxic effector by its cognate metaeffector promotes Legionella pneumophila virulence

“…Our data, in the context of previously published studies (11, 12), suggest that SidI’s target is conserved between host and pathogen. Recent phylogenetic analysis suggests ancient and extensive co-evolution between the order Legionellales, which includes Legionella spp., and unicellular eukaryotes (41). Thus, metaeffectors may represent an ancient mechanism evolved by pathogenic bacteria for adaptation to eukaryotic hosts.…”

The inside scoop: Comparative genomics of two intranuclear bacteria, “Candidatus Berkiella cookevillensis” and “Candidatus Berkiella aquae”

“…analyses, CC99 and HT99 have been classified as separate novel species forming distinct taxonomic lineages within the Coxiellaceae family of the order Legionellales and class Gammaproteobacteria [17]. However, recent phylogenetic analysis that included more than 100 Gammaproteobacteria genomes using concatenated amino acid alignment of 109 proteins has classified CC99 and HT99 as a separate distinct family outside Coxiellaceae [18]. Both bacteria show a close 16S rRNA similarity each other (~94%) and to the intracellular pathogens Coxiella burnetii (~90-91%) and L. pneumophila (~88%) [17], the causative agents of the zoonotic disease Q fever [19] and Legionnaires' disease [20], respectively.…”