Source: PENNSYLVANIA STATE UNIVERSITY submitted to NRP
THE MOLECULAR BASIS OF SURVIVAL TO MEMBRANE-TARGETING BACTERIAL CONTROL METHODS, AND IMPLICATIONS FOR DISEASE CONTROL
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1027965
Grant No.
2022-67013-36276
Cumulative Award Amt.
$682,500.00
Proposal No.
2021-08463
Multistate No.
(N/A)
Project Start Date
Jan 1, 2022
Project End Date
Dec 31, 2025
Grant Year
2022
Program Code
[A1112]- Pests and Beneficial Species in Agricultural Production Systems
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
408 Old Main
UNIVERSITY PARK,PA 16802-1505
Performing Department
Plant Pathology and Environmen
Non Technical Summary
Disruption of bacterial outer membranes (OM) by antimicrobial agents is a major area of promise for biocontrol and plant disease resistance. Examples include bacterially produced toxins, termed tailocins, which show excellent promise for specific and engineerable prophylaxis. Additionally, LPS targeting antimicrobial peptides (AMP) are the major difference between Huanglongbing (HLB) resistant and susceptible plants. Indeed, plants are known to produce an array of AMPs that kill microbes through membrane disruption. Despite this promise, we've shown that bacteria can enter temporary physiological states that make them tolerant to membrane-active treatments, a phenomenon termed persistence. Such persistence complicates the effectiveness of these treatments. Moreover, modeling has predicted for many antimicrobials, including those that are OM-targeting, that persistence can speed the evolution of resistance, further impeding our ability to deploy these agents for long-term control. Thus, understanding the prevalence and mechanisms of survival to OM-targeting treatments will be critical for determining under what conditions these treatments will be durable and effective, and for designing resistance mitigation strategies. We aim to 1) understand the physiology and genetics that underlie bacterial persistence to multiple OM-targeting agents, 2) determine whether there is overlap in persistence mechanisms to distinct OM-targeting agents, and 3) assess empirically whether increased persistence can result in increased rates of resistance, as well as how persistence contributes to treatment survival in a plant host environment. The results of this research will improve our ability to predict the potential outcomes of OM-targeting antimicrobials and modify treatment strategies to ensure their long-term effectiveness.
Animal Health Component
25%
Research Effort Categories
Basic
75%
Applied
25%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21240101100100%
Knowledge Area
212 - Pathogens and Nematodes Affecting Plants;

Subject Of Investigation
4010 - Bacteria;

Field Of Science
1100 - Bacteriology;
Goals / Objectives
The goal of this project is to identify the extent, genetic mechanisms, and potential agricultural consequences of persistence to membrane-disrupting antimicrobials.The three aims will address three major questions:Q1:Do pathogenic bacteria have persistent subpopulations to multiple major classes of membrane disruptors, and are these populations distinct or overlapping?Q2:What genetic pathways mediate persistence to different membrane-disrupting antimicrobials?AndQ3:Could persistence to membrane disrupting compounds lead to treatment failure and resistance in agricultural contexts?We will address these questions in the modelPphsystem by characterizing the phenotypes of persisters to diverse treatments (Aim 1), characterizing gene expression patterns and mutations associated with persistence (Aim 2), and by determining the diversity of persistence levels across diverseP. syringaepathovars, as well as whether persistence likely contributes to fitness or leads to resistance in the host plant context (Aim 3). The project will result in an understanding of how pathogen populations withstand different types of membrane disruption, and in turn which treatments could be used in combination to mitigate these effects. Our long-term goal is, through understanding the prevalence and mechanisms of these survival strategies, to maximize the efficacy of membrane-disrupting antimicrobials and minimize the potential for resistance.?
Project Methods
The project will be conducted using a combination of microbiological, bioinformatic, and plant pathological approaches.Aim 1 will be carried out using a combination of laboratory culture, fluorescent redox labelling, and single cell microfluidics. Specifically, we will use culture- and plant-based bacterial enumeration to quantify the effect of antimicrobial resistance; redox reporters will be combined with microfluidic cell sorting to determine the cell physiology underlying persistence. Results of this research will be delivered to target audiences through peer-reviewed publication and scientific presentation. Success associated with this objective will be measured through the production of a peer-reviewed publicationAim 2 will combine microfluidic cell sorting with transcriptomic sequencing to characterize the transcriptional profiles of persisters cells, which will be compared to non-persister cells sorted from the same parent population. Additionally, we will select for and recover mutants exhibiting increased persistence against each of the membrane-targeting antimicrobials to gain deeper insight into the genetics underlying persistence. Results of this research will be delivered to target audiences through peer-reviewed publication and scientific presentation. Success associated with this objective will be measured through the production of a peer-reviewed publication, as well as generating a collection of 10+ mutant isolates that are increased in persistence against each antimicrobial.Aim 3 will combine laboratory and plant-based microbiological techniques to assess the diversity of natural levels of persistence acrossP. syringae, as well as the effect of persistence in in planta survival and proliferation. Additionally, this aim will use an experimental evolution approach to determine the effect of persistence on the acquisition of resistance. Results of this research will be delivered to target audiences through peer-reviewed publication and scientific presentation. Success associated with this objective will be measured through the production of a peer-reviewed publication.

Progress 01/01/23 to 12/31/23

Outputs
Target Audience:The target audiences reached during this reporting period include scientific researchers from industry, government, and academia. Changes/Problems:Change of institutions for the Chang lab, as well as turnover of the postdoc working in the Hockett lab has resulted in slowed progress. What opportunities for training and professional development has the project provided?Training ofa technician, a postdoc, and a graduate student was accomplished. How have the results been disseminated to communities of interest?These results have not yet been disseminated to a community of interest. What do you plan to do during the next reporting period to accomplish the goals?During the next reporting period, we plan to identify the high persister mutations contributing toward tailocin and MtDef4 persistence. Additionally, we will aim to isolate persisters for RNAseq analysis. Finally, we will inoculate host plants with high persister mutants to assess whether the high persistence is observable in a plant context.

Impacts
What was accomplished under these goals? The Triplett lab isolated multiple high persister mutants to both tailocin and MtDef4. These mutants have been sequenced and the Hockett lab is currently working to identify the causative mutations underlying the phenotypes.

Publications


    Progress 01/01/22 to 12/31/22

    Outputs
    Target Audience:Target audiences reached during this reporting period include microbiological scientists at Montana State University through a thesis defense by an MS student working on this project. Additionally, the wider scientific community was reached through publication of the MS thesis. Changes/Problems:The Hockett lab has been unable to reliably recover colistin resistant mutants. We will move forward with other aspects of objective 3 (including starting to perform the in planta experiments), and return to this sub-objective if funds and time allow. What opportunities for training and professional development has the project provided?Two postdocs, one graduate student, and one undergraduate student have been trained as a result of this project. This includes one MS student graduating with this work as the central feature of theirthesis. How have the results been disseminated to communities of interest?This work has been reported through a thesis defense seminar and publicly available thesis to the scientific community. What do you plan to do during the next reporting period to accomplish the goals?The Chang lab: Aim 1: Utilize treatment, staining, and encapsulation protocol to encapsulate tailocin treated Pph at the single-cell level for subsequent laser-induced fluorescent analysis. Analyze fluorescent signals of single cells encapsulated into droplets to detect and confirm for the presence of persister cells. Aim 2:Sort droplets at the single cell level following antimicrobial treatmentand staining to isolate surviving cells for transcriptome sequencing of persister cells and to correlate a cells ability to regrow on non-selective media to its fluorescent signal. The Triplett lab: Work in the Triplett lab in the next reporting period will focus on isolating mutations that influence persistence to these treatments. The Hockett lab: The Hockett lab will move forward with completing assessment of tailocin persistnece levels for the remaining pathovars. Additionally, we will assess whether persistence levels to MtDef4 correlate with resistance emergence.

    Impacts
    What was accomplished under these goals? Toward objective 1, experiments in the Triplett lab confirmed that Pph forms persister cells to both colistin and MtDef4, and that persistence levels increase in later bacterial growth phases (Objective 1.1). Simultaneous and sequential cross-tolerance assays were performed as proposed in Obj. 1.2. While colistin eliminated 90% of persister cells remaining after MtDef4 treatment, tailocin did not have any effect on MtDef4 survivors. Furthermore, simultaneous treatment of Pph with tailocin and MtDef4 was no more effective than each treatment alone. These results suggest that persistence to tailocin and MtDef4 work through overlapping mechanisms, which are distinct from the mechanism of persistence to colistin. Protocols for the treatment, staining, and encapsulation of Pph were developed to allow the single-cell encapsulation of treated and fluorescently labeled cells into 25mm microfluidic droplets. These protocols were applied to the fluorescent characterization of Pph at three concentrations of carbonyl cyanide m-chlorophenylhydrazone (0.5x, 5x, and 50xthe minimum inhibitory concentration (20mg/ml)) which resulted in 6.2%, 10.2%, and 88.6% cell death, respectively. Regarding aim 2, adielectrophoresis-based microfluidic platform was demonstrated to have the ability to sort 25mm microfluidic droplets based on two colors representing the staining pattern used to identify tailocin persister cells in Pph(previous work has shown that tailocin persisters exhibit staining with the redox reporter Redox Sensor Green but remained impermeable to the membrane permeability stain Draq7). The microfluidic sorter was also demonstrated to have the ability to sort droplets over a range of fluorescent signals in one color. Regarding aim 3, the Hockett lab has testedall 14pathovars for their persistence levels to both colistin and MtDef4. The pathovars can be grouped into three general categories, those that exhibited little to no killing when stationary phase cells were exposed to either antimicrobial, those that exhibited an initial level of rapid killing followed by a slower death curve, and those that were rapidly killed over the course of 5 hours of exposure.The Hockett lab has also begun assessing the persistence levels to tailocin for the 14 pathovars. Multiple attempts to quantify colistin resistance have been made, but we have been unsuccessful in recovering a confirmed colisitin resistant mutant (see changes/problems).

    Publications

    • Type: Theses/Dissertations Status: Accepted Year Published: 2023 Citation: Citation hasn't been generated yet.