Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system

Dr, Ortega; Subramanian, Poorna; Mann, Petra; Kjær, Andreas; Chen, S; Kj, Watts; Pirbadian, Sahand; Chen, Da; Kooger, Romain; Mg, Kalyuzhnaya; Ringgaard, Simon; Briegel, Ariane; Jensen, GJ

doi:10.1101/653600

Cited by 3 publications

(4 citation statements)

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“…The domain architecture of the signaling region of Tlp4a is similar to that of the Aer2-like chemoreceptor found in Methylomicrobium alcaliphilum (MEALZ_2872) (Fig. S4) and for which a homology model is available (33). Using the cytoplasmic region of the M. alcalyphilum Aer-2-like as a template (Fig.…”

Section: Resultsmentioning

confidence: 67%

Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output

O’Neal

Gullett

Aksenova

et al. 2019

mBio

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Most chemotactic motile bacteria possess multiple chemotaxis signaling systems, the functions of which are not well characterized. Chemotaxis signaling is initiated by chemoreceptors that assemble as large arrays, together with chemotaxis coupling proteins (CheW) and histidine kinase proteins (CheA), which form a baseplate with the cytoplasmic tips of receptors. These cell pole-localized arrays mediate sensing, signaling, and signal amplification during chemotaxis responses. Membrane-bound chemoreceptors with different cytoplasmic domain lengths segregate into distinct arrays. Here, we show that a bacterium, Azospirillum brasilense, which utilizes two chemotaxis signaling systems controlling distinct motility parameters, coordinates its chemotactic responses through the production of two separate membrane-bound chemoreceptor arrays by mixing paralogs within chemotaxis baseplates. The polar localization of chemoreceptors of different length classes is maintained in strains that had baseplate signaling proteins from either chemotaxis system but was lost when both systems were deleted. Chemotaxis proteins (CheA and CheW) from each of the chemotaxis signaling systems (Che1 and Che4) could physically interact with one another, and chemoreceptors from both classes present in A. brasilense could interact with Che1 and Che4 proteins. The assembly of paralogs from distinct chemotaxis pathways into baseplates provides a straightforward mechanism for coordinating signaling from distinct pathways, which we predict is not unique to this system given the propensity of chemotaxis systems for horizontal gene transfer. IMPORTANCE The assembly of chemotaxis receptors and signaling proteins into polar arrays is universal in motile chemotactic bacteria. Comparative genome analyses indicate that most motile bacteria possess multiple chemotaxis signaling systems, and experimental evidence suggests that signaling from distinct chemotaxis systems is integrated. Here, we identify one such mechanism. We show that paralogs from two chemotaxis systems assemble together into chemoreceptor arrays, forming baseplates comprised of proteins from both chemotaxis systems. These mixed arrays provide a straightforward mechanism for signal integration and coordinated response output from distinct chemotaxis systems. Given that most chemotactic bacteria encode multiple chemotaxis systems and the propensity for these systems to be laterally transferred, this mechanism may be common to ensure chemotaxis signal integration occurs.

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Section: Resultsmentioning

confidence: 67%

Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output

O’Neal

Gullett

Aksenova

et al. 2019

mBio

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“…Aer2‐containing systems are ancestral to the E. coli chemotaxis system (Ortega et al, 2020). This allows Aer2 receptors, like Pa Aer2 and Vc Aer2, to hijack E. coli chemotaxis and initiate cell tumbling in the presence of O 2 (Greer‐Phillips et al, 2018; Watts et al, 2011).…”

Section: Resultsmentioning

confidence: 99%

“…Notably, Aer2‐containing systems represent two distinct stages in the evolutionary transition of F7 systems into the E. coli chemotaxis system. V. cholerae che3 and V. vulnificus che2 represent stage 1, whereas P. aeruginosa che2 represents stage 2 (Ortega et al, 2020). To determine if Vv Aer2 can induce a behavioral response in E. coli , aer2 ( VVA1688 ) was cloned from V. vulnificus YJ016 gDNA and expressed from pProEX in otherwise chemoreceptorless E. coli BT3388.…”

Section: Resultsmentioning

confidence: 99%

“…The HAMP1 domain of Pa Aer2 was recently shown to be a protein clustering and localization determinant (Anaya et al, 2022). Such a role for the PAS1 domains of Vc Aer2 and Vv Aer2 is conceivable given that Aer2 receptors form membrane‐associated polar clusters (Ortega et al, 2020). Further PAS control might be provided by direct interactions between PAS and a different protein, as has been shown for CckA and DivL from Caulobacter crescentus (Mann & Shapiro, 2018).…”

Section: Discussionmentioning

confidence: 99%

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The Aer2 chemoreceptor from Vibrio vulnificus is a tri‐PAS‐heme oxygen sensor

Stuffle

Suzuki

Orillard

et al. 2022

Molecular Microbiology

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The marine pathogen Vibrio vulnificus senses and responds to environmental stimuli via two chemosensory systems and 42–53 chemoreceptors. Here, we present an analysis of the V. vulnificus Aer2 chemoreceptor, VvAer2, which is the first V. vulnificus chemoreceptor to be characterized. VvAer2 is related to the Aer2 receptors of other gammaproteobacteria, but uncharacteristically contains three PAS domains (PAS1‐3), rather than one or two. Using an E. coli chemotaxis hijack assay, we determined that VvAer2, like other Aer2 receptors, senses and responds to O2. All three VvAer2 PAS domains bound pentacoordinate b‐type heme and exhibited similar O2 affinities. PAS2 and PAS3 both stabilized O2 via conserved Iβ‐Trp residues, but PAS1, which was easily oxidized in vitro, was unaffected by Iβ‐Trp replacement. Our results support a model in which PAS1 is largely dispensable for O2‐mediated signaling, whereas PAS2 modulates PAS3 signaling, and PAS3 signals to the downstream domains. Each PAS domain appeared to be positionally optimized, because PAS swapping caused altered signaling properties, and neither PAS1 nor PAS2 could replace PAS3. Our findings strengthen previous conclusions that Aer2 receptors are O2 sensors, but with distinct N‐terminal domain arrangements that facilitate, modulate and tune responses based on environmental signals.

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Phylogenetic Characterization of the Energy-taxis Receptor Aer inPseudomonasand Phenotypic Characterization inP. pseudoalcaligenesKF707

Booth

Turner

2016

Preprint

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15Chemotaxis allows bacteria to sense gradients in their environment and respond by 16 directing their swimming. Aer is a receptor that, instead of responding to a specific 17 chemoattractant, allows bacteria to sense cellular energy levels and move towards favourable 18 environments. In Pseudomonas, the number of apparent Aer homologs differs between the only 19 two species it had been characterized in, P. aeruginosa and P. putida. Here we combined 20 bioinformatic approaches with deletional mutagenesis in P. pseudoalcaligenes KF707 to further 21 characterize Aer. It was determined that the number of Aer homologs varies between 0-4 22 throughout the Pseudomonas genus, and they were phylogenetically classified into 5 subgroups. 23 We also used sequence analysis to show that these homologous receptors differ in their HAMP 24 signal transduction domains. Genetic analysis also indicated that some Aer homologs have likely 25 been subject to horizontal transfer. P. pseudoalcaligenes KF707 was unique among species for 26 having three Aer homologs as well as the receptors CttP and McpB. Phenotypic characterization 27 in this species showed the most prevalent homolog of Aer was key, but not essential for energy-28 taxis. This study demonstrates that energy-taxis in Pseudomonas varies between species and 29 provides a new naming convention and associated phylogenetic details for Aer chemoreceptors. 30 31 73 the Pseudomonas genus with a genetic knockout characterization of three Aer homologs, McpB 74 and CttP in P. pseudoalcaligenes KF707. A phylogeny of Aer was built using sequences 75 obtained from 65 Pseudomonas species providing insight into the distribution throughout the 76 genus and enabling the definition of five 'Aer' groups. Only P. pseudoalcaligenes KF707 had 77 5 the unique feature of possessing three Aer homologs, McpB and CttP making it the ideal 78 candidate to investigate if these receptors had related functions. Using single and combinatory 79 deletion mutants, we found that the most common Pseudomonas Aer homolog had the most 80 influence on energy-taxis. Together these results provide a definition of the Aer energy-taxis 81 receptor as a family with varied distribution in Pseudomonas and implicate the most common 82 Aer homolog as the primary energy-taxis receptor in P. pseudoalcaligenes KF707. 83 84 Results 85To investigate how the number of Aer-like receptors, differences in their amino acid 86 sequences and how they are related phylogenetically, Aer sequences from 65 Pseudomonas 87 species were analyzed. Species with completely sequenced genomes were selected, but for those 88 with many strains only a few representatives that have been highly studied were included (e.g. P. 89 aeruginosa). Species with incomplete (draft) sequences were also included in an attempt to 90 ensure representation from all major Pseudomonas clades [16, 17]. 144 protein sequences were 91 obtained from the NCBI database using the P. aeruginosa PA01 Aer sequence (NP_250252.1) as 92 a BLAST [21] query sequence. All hits ...

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Repurposing a macromolecular machine: Architecture and evolution of the F7 chemosensory system

Cited by 3 publications

References 71 publications

Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output

Distinct Chemotaxis Protein Paralogs Assemble into Chemoreceptor Signaling Arrays To Coordinate Signaling Output

The Aer2 chemoreceptor from Vibrio vulnificus is a tri‐PAS‐heme oxygen sensor

Phylogenetic Characterization of the Energy-taxis Receptor Aer inPseudomonasand Phenotypic Characterization inP. pseudoalcaligenesKF707

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