A PilZ-Containing Chemotaxis Receptor Mediates Oxygen and Wheat Root Sensing in Azospirillum brasilense

Abstract

Chemotactic bacteria sense environmental changes via dedicated receptors that bind to extra- or intracellular cues and relay this signal to ultimately alter direction of movement toward beneficial cues and away from harmful environments. In complex environments, such as the rhizosphere, bacteria must be able to sense and integrate diverse cues. Azospirillum brasilense is a microaerophilic motile bacterium that promotes growth of cereals and grains. Root surface colonization is a prerequisite for the beneficial effects on plant growth but how motile A. brasilense navigates the rhizosphere is poorly studied. Previously only 2 out of 51 A. brasilense chemotaxis receptors have been characterized, AerC and Tlp1, and only Tlp1 was found to be essential for wheat root colonization. Here we describe another chemotaxis receptor, named Aer, that is homologous to the Escherichia coli Aer receptor, likely possesses an FAD cofactor and is involved in aerotaxis (taxis in an air gradient). We also found that the A. brasilense Aer contributes to sensing chemical gradients originating from wheat roots. In addition to A. brasilense Aer having a putative N-terminal FAD-binding PAS domain, it possesses a C-terminal PilZ domain that contains all the conserved residues for binding c-di-GMP. Mutants lacking the PilZ domain of Aer are altered in aerotaxis and are completely null in wheat root colonization and they also fail to sense gradients originating from wheat roots. The PilZ domain of Aer is also vital in integrating Aer signaling with signaling from other chemotaxis receptors to sense gradients from wheat root surfaces and colonizing wheat root surfaces.

Control of mRNA translation by dynamic ribosome modification

“…Bacterial adaptation to complex natural environments is controlled by an intricate series of connected signalling pathways that function both within individual cells and on the microbial community as a whole [11,14,26]. In addition to extensive transcriptional [6,11] and protein functional regulation [12], control of mRNA translation is critical for effective colonisation of plant rhizospheres [7]. In this study we characterise the RimABK pathway in Pseudomonas fluorescens and present evidence for the role that this novel translational regulatory system plays during bacterial adaptation to the rhizosphere environment through specific, controlled modification of a ribosomal protein.…”

“…This requires an interconnected network of signal transduction systems functioning at multiple regulatory levels, including gene transcription [6], modulation of translational activity [7] and changes in protein function [8]. The cyclic-di-GMP (cdG) signalling network mediates the switch between motile and sessile lifestyles in many bacterial species [9] and is a key regulator of rhizosphere colonisation in multiple plant-associated microbes [10][11][12][13]. CdG signalling in Pseudomonas forms a highly complex, non-linear and pleiotropic network, with multiple connections to other signalling systems and phenotypic outputs that vary profoundly in response to environmental cues [14,15].…”

Structural Conservation and Diversity of PilZ-Related Domains

“…2). Based on sequence comparisons, it has also been predicted in PilZ-containing chemotaxis receptors Tlp1 and Aer from Azospirillum brasilense (29,30), Ser/Thr-type protein kinase Pkn1 (MXAN_1467) from Myxococcus xanthus (61), and many other PilZ fusion proteins. This helix is characterized by a large number of charged amino acid residues, particularly Arg and Lys, which makes it a prime candidate for protein-protein interactions.…”

Second messenger control of mRNA translation by dynamic ribosome modification

“…Bacterial adaptation to complex natural environments is controlled by an intricate series of connected signalling pathways that function both within individual cells and on the microbial community as a whole (22, 25, 44). In addition to extensive transcriptional (17, 22) and protein functional regulation (23), control of mRNA translation is critical for effective colonisation of plant rhizospheres (18). In this study we characterise the RimABK pathway in Pseudomonas fluorescens ; a novel translational regulatory system that controls bacterial adaptation to the rhizosphere environment through specific, controlled modification of a ribosomal protein.…”