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Evolutionary history expands the range of signaling interactions in hybrid multikinase networks.

ABSTRACT: Two-component systems (TCSs) are ubiquitous signaling pathways, typically comprising a sensory histidine kinase (HK) and a response regulator, which communicate via intermolecular kinase-to-receiver domain phosphotransfer. Hybrid HKs constitute non-canonical TCS signaling pathways, with transmitter and receiver domains within a single protein communicating via intramolecular phosphotransfer. Here, we report how evolutionary relationships between hybrid HKs can be used as predictors of potential intermolecular and intramolecular interactions ('phylogenetic promiscuity'). We used domain-swap genes chimeras to investigate the specificity of phosphotransfer within hybrid HKs of the GacS-GacA multikinase network of Pseudomonas brassicacearum. The receiver domain of GacS was replaced with those from nine donor hybrid HKs. Three chimeras with receivers from other hybrid HKs demonstrated correct functioning through complementation of a gacS mutant, which was dependent on strains having a functional gacA. Formation of functional chimeras was predictable on the basis of evolutionary heritage, and raises the possibility that HKs sharing a common ancestor with GacS might remain components of the contemporary GacS network. The results also demonstrate that understanding the evolutionary heritage of signaling domains in sophisticated networks allows their rational rewiring by simple domain transplantation, with implications for the creation of designer networks and inference of functional interactions.

SUBMITTER: Ortet P

PROVIDER: S-EPMC8175716 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundFamily Rhinolophidae (horseshoe bats), Hipposideridae (leaf-nosed bats) and Rhinonycteridae (trident bats) are exclusively distributed in the Old-World, and their biogeography reflects the complex historic geological events throughout the Cenozoic. Here we investigated the origin of these families and unravel the conflicting family origin theories using a high resolution tree covering taxa from each zoogeographic realm from Africa to Australia. Ancestral range estimations were performed using a probabilistic approach implemented in BioGeoBEARS with subset analysis per biogeographic range [Old-World as whole, Australia-Oriental-Oceania (AOO) and Afrotropical-Madagascar-Palearctic (AMP)].ResultOur result supports an Oriental origin for Rhinolophidae, whereas Hipposideridae originated from the Oriental and African regions in concordance with fossil evidence of both families. The fossil evidence indicates that Hipposideridae has diversified across Eurasia and the Afro-Arabian region since the Middle Eocene. Meanwhile, Rhinonycteridae (the sister family of Hipposideridae) appears to have originated from the Africa region splitting from the common ancestor with Hipposideridae in Africa. Indomalaya is the center of origin of Rhinolophidae AOO lineages, and Indomalayan + Philippines appears to be center of origin of Hipposideridae AOO lineage indicating allopatric speciation and may have involved jump-dispersal (founder-event) speciation within AOO lineage. Wallacea and the Philippines may have been used as stepping stones for dispersal towards Oceania and Australia from the Oriental region. Multiple colonization events via different routes may have occurred in the Philippines (i.e., Palawan and Wallacea) since the Late Miocene. The colonization of Rhinolophidae towards Africa from Asia coincided with the estimated time of Tethys Ocean closure around the Oligocene to Miocene (around 27 Ma), allowing species to disperse via the Arabian Peninsula. Additionally, the number of potential cryptic species in Rhinolophidae in Southeast Asia may have increased since Plio-Pleistocene and late Miocene.ConclusionOverall, we conclude an Oriental origin for Rhinolophidae, and Oriental + African for Hipposideridae. The result demonstrates that complex historical events, in addition to species specific ecomorphology and specialization of ecological niches may shape current distributions.

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Evolutionary history expands the range of signaling interactions in hybrid multikinase networks.

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