Abstract
Adaptive radiation is the rapid origination of multiple species from a single ancestor as the result of concurrent adaptation to disparate environments. This fundamental evolutionary process is considered to be responsible for the genesis of a great portion of the diversity of life. Bacteria have evolved enormous biological diversity by exploiting an exceptional range of environments, yet diversification of bacteria via adaptive radiation has been documented in a few cases only and the underlying molecular mechanisms are largely unknown. Here we show a compelling example of adaptive radiation in pathogenic bacteria and reveal their genetic basis. Our evolutionary genomic analyses of the α-proteobacterial genus Bartonella uncover two parallel adaptive radiations within these host-restricted mammalian pathogens. We identify a horizontally-acquired protein secretion system, which has evolved to target specific bacterial effector proteins into host cells as the evolutionary key innovation triggering these parallel adaptive radiations. We show that the functional versatility and adaptive potential of the VirB type IV secretion system (T4SS), and thereby translocated Bartonella effector proteins (Beps), evolved in parallel in the two lineages prior to their radiations. Independent chromosomal fixation of the virB operon and consecutive rounds of lineage-specific bep gene duplications followed by their functional diversification characterize these parallel evolutionary trajectories. Whereas most Beps maintained their ancestral domain constitution, strikingly, a novel type of effector protein emerged convergently in both lineages. This resulted in similar arrays of host cell-targeted effector proteins in the two lineages of Bartonella as the basis of their independent radiation. The parallel molecular evolution of the VirB/Bep system displays a striking example of a key innovation involved in independent adaptive processes and the emergence of bacterial pathogens. Furthermore, our study highlights the remarkable evolvability of T4SSs and their effector proteins, explaining their broad application in bacterial interactions with the environment.
Highlights
Adaptation to different ecological niches can lead to rapid diversification of a single ancestor into an array of distinct species or ecotypes
This study revealed that two type IV secretion systems (T4SS), Trw and VirB, which are essential for host interaction at different stages of the infection cycle represent the few colonization factors exclusively found in the most species rich sub-lineages of bartonellae
As the chromosomal organization implicates different evolutionary histories of the VirB T4SS in the two radiating lineages, we investigated the relation among the effector proteins translocated by this secretion system
Summary
Adaptation to different ecological niches can lead to rapid diversification of a single ancestor into an array of distinct species or ecotypes. This process, called adaptive radiation, typically occurs after the arrival of a founding population in a novel environment with unoccupied ecological niches (‘ecological opportunity’) and/or by the acquisition of a novel trait (‘evolutionary key innovation’) allowing the exploitation of so far unapproachable niches [1]. One of the most fascinating aspects of adaptive radiation is the frequent occurrence of evolutionary parallelism resulting in independent adaptation to same ecological niches [8,9,10]. Lineages that radiate in parallel are of great value to study the molecular basis of adaptation and their independent evolutionary
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