Evolution of monomodular all-helical receptor ligand-binding domains from bimodular ancestors

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Bacterial chemotaxis is essential for environmental adaptation and host interaction. To this end, bacteria have evolved exceptionally broad chemosensory capacities, with few apparent constraints on ligand structure or size. These capacities are determined by the extraordinary diversity of chemoreceptor ligand-binding domains (LBDs), which recognize chemoeffectors and evolve rapidly to acquire new functions. Many LBDs have complex architectures, often comprising multiple ligand-binding modules. Among chemoreceptor LBDs, members of the all-helical class are widespread and can contain one, two, or three stacked four-helix bundle (4HB) modules. Here, using phylogenomic, structural, and biochemical approaches, we identify a novel monomodular all-helical LBD family, termed 4HB_HD (4HB_HBM-derived), most likely originated from the bimodular all-helical HBM LBD by the loss of its membrane-distal module. A representative family member, PcpI of Pseudomonas putida, binds the plant hormones salicylate and indole-3-acetic acid and mediates chemotaxis toward these compounds. Comparison with the inferred bimodular ancestor, aPcpI, revealed that binds the phytohormones recognized by PcpI via both the membrane-distal and membrane-proximal modules, and additionally recognizes citrate through the membrane-distal module. Despite their distinct chemical structures, these ligands bind to the same site within the membrane-distal module, highlighting structural flexibility as a mechanism for expanding receptor specificity. Structural analyses further show that PcpI-LBD closely superimposes with the membrane-proximal module of aPcpI-LBD and provide a structural rationale for its inability to bind citrate. Together, our results show that modular reduction does not necessarily compromise function and illustrate how rearrangement of ligand-binding modules can drive the microbial evolution of inter-kingdom signal detection.

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