Source: AUBURN UNIVERSITY submitted to
INVESTIGATION OF VACCINATION AND DISEASE SUSCEPTIBILITY OF LARGEMOUTH BASS FRY DURING THE EARLY REARING STAGES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
ACTIVE
Funding Source
Reporting Frequency
Annual
Accession No.
1030490
Grant No.
2023-70007-40201
Cumulative Award Amt.
$300,000.00
Proposal No.
2022-06028
Multistate No.
(N/A)
Project Start Date
Jul 1, 2023
Project End Date
Jun 30, 2025
Grant Year
2023
Program Code
[AQUA]- Aquaculture Research
Project Director
Bruce, T.
Recipient Organization
AUBURN UNIVERSITY
108 M. WHITE SMITH HALL
AUBURN,AL 36849
Performing Department
SCHOOL OF FISHERIES
Non Technical Summary
Largemouth bass is an up-and-coming cultured fish species in the United States, with greatpotential as a production foodfish. The early life stages remain to be better clarified for optimized production in both pond and indoor rearing systems. Largemouth bass are susceptible to bacterial diseases during the early rearing periods, and there is limited information on therapeutics for producers. A major bacterial pathogen is Aeromonasspp., which cause motileAeromonassepticemia. These bacteria are often synonymous with rearing stressors and can lead to high levels of mortality. As such, this dynamic project team aims to investigate disease susceptibility and immunological responses of largemouth bass during these critical production stages. Specifically, the outlined project objectives are to 1) Develop and evaluate an immersion-based challenge model for motileAeromonassepticemia (MAS;Aeromonas hydrophilaandAeromonas veronii) in largemouth bass; 2) Characterize disease susceptibility and immune responses to MAS infections in largemouth bass fry and fingerling across the early rearing stages; and 3) Assess the efficacy and potential for killed, immersion-basedA. hydrophilaandA. veroniibacterins when administered at various timepoints within the early life stages, along with potential cross-protection. The research team will translate research findings for commercial largemouth bass producers and the projectoutcomes will be used to enhance U.S. foodfish production for domestic food security.
Animal Health Component
80%
Research Effort Categories
Basic
20%
Applied
80%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
3110810109040%
3110810104010%
3110810110050%
Knowledge Area
311 - Animal Diseases;

Subject Of Investigation
0810 - Finfish;

Field Of Science
1090 - Immunology; 1040 - Molecular biology; 1100 - Bacteriology;
Goals / Objectives
The team's long-term goal is to develop disease mitigation strategies and define aspects of the LMB immune response to bacterial pathogens and vaccination during the critical early rearing periods. As such, we aim to 1)Develop and evaluate an immersion-based challenge model for MAS (AeromonashydrophilaandAeromonas veronii) in LMB; 2)Characterize disease susceptibility, gut microbiota, and immune responses to MASinfections in LMB fry and fingerling across the early rearing stages;and 3)Assess the efficacy and potential for killed, immersion-basedA. hydrophilaandA. veroniibacterins when administered at various time points within the early life stages, along with potential cross-protectionTogether, these approaches will give the aquaculture sector a scientific toolbox to combat diseases that are reoccurring in LMB farms.
Project Methods
Northern LMB embryos or sac fry will be transported to SFAAS, where they will be reared at Dr. Peatman's facility, in a land-based raceway system (4000 L tanks). This rearing strategy will optimize growth and development over the project period.LMB will be reared on standard commercial diets. For experimental challenges, a total of 4 virulent isolates (twoA. hydrophilaand twoA. veronii) obtained from Dr. Bruce's Lab or the USDA-ARS AAHRU will be revived from glycerol cryostock on tryptic soy agar (TSA) plates at 24°C. A single colony pick will be used to scale the culture to 1L volumes in tryptic soy broth (TSB) and a selected optical density at 600 nm (i.e., OD600), based on pilot culture work. Before initiating preliminary challenges, bacterial titration curves will be prepared to discern growth mechanics and colony-forming units per mL (CFU mL-1) for each of the four strains. For initial virulence and delivery testing, fish will be exposed to 4 dilutions (104to 107CFU mL-1) using triplicate tanks of 20 fish tank-1(65L tanks) for each dilution, with an initial screening size of 5-10 g, a tank volume of 10 L (100 mL of inoculum added), and a temperature of 24°C. The fish will be subjected to the static immersion challenge for 1h with aeration via air stones before flows (0.3-0.5 L min-1) are restored, and tank volumes are filled to 20 L. Triplicate tanks of mock-challenged fish (sterile TSB only) will also be included. Mortality will be assessed for a total of 10d post-initiation. Mortalities will be collected every 6-12 h, and spleen and posterior kidney tissues will be streaked on TSA for pathogen reisolation.Depending on the outcomes of the first round of immersion challenges, selected modifications to the challenge protocol will then be applied, as previously documented in virulentAeromonas hydrophilachallenges in channel catfish. First, skin mucus surrounding the dorsal fin will be removed with light abrasions using a flat spatula immediately prior to immersion (Li et al., 2013). The entire challenge process above will be repeated with varied inoculum doses. If this approach again proves unsuccessful in generating mortality, a clipping of a portion of the soft dorsal fin will be used, like the model developed by Zhang et al. (2016). For this procedure, LMB will be lightly anesthetized with 80 mg L-1of MS-222 and exposed to the pathogen immediately following the clip. If desirable cumulative percent mortality (CPM) of >50 % is achieved, a final modification step, incorporating the use of an iron-chelating xenosiderophore (deferoxamine mesylate; 0.4 mM), will be added during the bacterial inoculum incubation to increase pathogen virulence (Peatman et al., 2018). At the completion of this objective, the top candidate strains (one forA. hydrophilaand one forA. veronii) will be used in the following project aims. This stepwise approach to expanding the immersion-based model will allow for a more natural route of infection, which results in high and rapid mortality.The second project aim will build upon the optimized disease challenge model described in Objective 1 and discern aspects of the ontogenic LMB immune response to pathogens over 6 months. As described above, LMB fry and fingerling will be reared over a period of 6 months. The fish will be stocked into a total of three rearing tanks for propagation. Starting as 1g fry, LMB will be exposed toA. hydrophilaandA. veroniipathogen challenges every month throughout this period (6 times). Prior to the challenge, a subset of the fry or fingerling will be evaluated for morphometric indices by Dr. Butts. These include total length, eye diameter, body area or depth, jaw length, and developmental deformities. At the same time, samples of intestinal tissue (distal intestines from 3 fish per tank, across 6 tanks) will be aseptically collected and flash-frozen in liquid nitrogen for 16S profiling of the V3 and V4 regions. Diet and water samples will also be captured at these time points. In addition to the samples collected for microbiome analyses, kidney (target head kidney) and spleen samples will also be collected and preserved in Zymo DNA/RNA Shield for gene expression analysis. Following the pre-challenge sampling, fish will be subjected to thein vivoAeromonasspp. immersion challenges. At the challenge completion, gut microbiota (and associated rearing water) and immune tissues will again be sampled. All challenges will incorporate triplicate tanks for each pathogen type, including a shared group of triplicate tanks as a mock-challenged group.All gut microbiota samples will be sent to a contract laboratory (Zymo Research, Irvine, CA) for DNA extraction, library preparation, and sequencing on the MiSeq platform. Read files will be generated and shared with the team for analysis. Alpha and beta diversity parameters will be evaluated.For gene expression, a total of five immune genes will be selected for RT-qPCR analyses. RNA will be extracted from the tissues using a Zymo Quick-RNA MiniKit (Zymo Research Inc., Irvine, CA), and purified RNA will be evaluated for quality and quantity on a Nanodrop Onecspectrophotometer (ThermoFisher Scientific, Waltham, MA). RNA concentrations will be uniformly adjusted, and template cDNA will be created using a High-capacity RNA-to-cDNA Kit (ThermoFisher Scientific, Waltham, MA). The generated cDNA will then be used in 10mL reactions with 2x PowerUp SYBR MasterMix (ThermoFisher Scientific, Waltham, MA) and runs conducted in triplicate on a Quantstudio 5 instrument (Applied Biosystems, Waltham, MA). Primers used in the reactions will be incorporated from previous LMB gene expression studies or designed using the NCBI database's Primer Designing Tool. All primers will be optimized prior to conducting the assays. Targets of interest will include genes such as interleukin 1b(il-1b), interleukin 8 (il-8), and tumor necrosis factora(tnf-a) (Yang et al. 2020a). Two housekeeping genes, such as elongation factor 1a(ef1a) or18S,will be implemented. Negative template control (NTC) will also be included in the RT-qPCR runs.The final project aim will involve the assessment of immersion-based vaccination againstA. hydrophilaandA. veronii. This phase will include vaccinations starting at the 1g fish size (time 0) and then two additional vaccinations at both 2 months and 4 months following. Formalin-killed (0.5% v/v) bacterins for each pathogen will be prepared according to methods by Wu et al. (2021). The bacterins will be administered to LMB for 0.5 h in a static bath, and the fish will be challenged at 30d post-vaccination with challenge timing based on preliminary reports of increased specific antibody levels (Wu et al., 2021). A sham-vaccinated group will also be included for eachA. hydrophilaorA. veroniistrain. Blood will be collected at 15 d and 30 d post-vaccination (from five fish per treatment group) and sera will be extracted to discernAeromonassp.-specific antibody titers, using a mouse anti-LMB IgM monoclonal antibody in an ELISA assay. Morphometric analyses will again be conducted to observe any notable developmental changes in response to vaccination. At the time of the immersion challenge (as in Objective 1), both vaccinated and sham-vaccinated fish for each of the two bacterins will be infected with bothA. hydrophila andA. veronii, along with mock-challenged groups (sterile TSB), and the challenge will be conducted for a period of 10 days. This approach will allow the team to investigate the potential cross-protective ability of each bacterin. In addition to thein vivo pathogen challenge trials to assess protection, vaccine-enabled immune responses and the influence of vaccination on the gut microbiota will be characterized using gene expression and 16S rRNA analyses.From the five fish collected for sera, spleens, kidneys, and sections of the distal intestine will also be aseptically extracted for these downstream analyses.

Progress 07/01/23 to 06/30/24

Outputs
Target Audience:This applied research project aims to translate findings directly to LMB producers and farmers looking to expand LMB production into their existing facilities. The target audience is scientists, producers, graduate students, extension specialists, and biotechnology/fish health companies. During this period, scientists, fish health companies, and graduate students were updated on the project's progress through presentations. Changes/Problems:While trying to complete the Objective 1 milestone, some issues were observed that delayed progress yet added an additional understanding ofA. hydrophilaandA. veroniiinfection dynamics in LMB.The following issues accounted for additional time spent on Objective 1 in our first year: 1. Difficulty identifying and culturing virulent isolates of MAS-causing species (Aeromonas veronii and Aeromonas hydrophila) a) Although we had manyAeromonasspp. to screen for use in the project, several species did not type asA. hydrophilaorA. veroniiusing traditional gene sequencing beyond16srRNA (i.e.,gyrBorrpoD). We remedied this by expanding isolate collection and whole genome sequencing a great deal of isolates. Further, we also foundA. hydrophilaisolates more difficult to locate. b) Another issue was that the virulence of our tested isolates differed greatly, so we had to conduct more in vivo assessments than anticipated. Significant time was dedicated to identifying growth dynamics with the use of siderophores (DFO&DPD). 2. Difficulty obtaining LMB due to time-specific rearing periods. a) Seasonal juvenile shortages delayed experiment periods for correctly sized LMB. b) The team also found a size-dependent influence on mortality when immersion-challenged with virulent isolates. 3.The challenge model optimization additionally needed more time to complete. a) Several months of research were dedicated to identifying a viable challenge model to receive desirable mortality rates. b) The lack of available literature on LMB immersion challenge models required additional tests to discern model inputs. Despite the additional time and inputs required to complete Objective 1, the research team identified a reproducible and standardized disease challenge model for MAS in LMB. Additionally, with the more detailed information obtained from this objective, the team will be able to compile a more comprehensive report on challenge model development and plans to construct an additional manuscript with these data. What opportunities for training and professional development has the project provided?Two M.S. students directly participate in the project and are mentored by the PD. The students had an opportunity to present at a fish health conference this year. How have the results been disseminated to communities of interest?One project presentationat the Western Fish Disease Workshop in 2024. What do you plan to do during the next reporting period to accomplish the goals?The team is on track to complete the proposed project objectives. Objective 2: The long-term study of LMB ontogeny began on July 13, 2024, when larval LMB were received.Bass were maintained and monitored until they were of size for the study (~1 g fish-1).The study was initiated on August 6, 2014, and that date was established as time 0.Every 30 days from that day, 18 LMB will be sampled for immune and intestinal tissues, and 180 LMB will be subjected to a disease challenge utilizing the previously established fin-clip model from Objective 1.After completion of the challenge, the survivors of the challenge will be sampled for gene expression and intestinal investigation.This pattern will continue for six disease challenges to understand the development of the LMB immune system and changes in immune response provided by gene expression analysis. Objective 3: During this period, the team designed and assembled a new state-of-the-art vaccination holding system capable of staging the study fish for sampling and pre-challenge isolation. The system comprises 8, 380 L tanks set with flow-through heated and dechlorinated water. The team also performed pilot bacterin preparations during this period to confirm vaccine sterility and dosages. We decided upon the addition of an immersion adjuvant for vaccination, as boosters were not included in the experimental approach, and this would be most applicable to enhancing the LMB immune response to the formalin-killed cells (FKCs). Using this pilot work, we successfully administered the first "time 0" bacterin to juvenile largemouth bass in August 2024.

Impacts
What was accomplished under these goals? Objective 1: The team completed Objective 1 during the first project period and sequenced several bacterial isolates collected from diagnostics cases (n=17) and included virulent Aeromonas hydrophila (vAh) from channel catfish (n=1) for virulence assessments. The16s,gyrB,andrpoDgenes were first screened for 11 isolates to obtain a preliminary PCR identification. We encountered issues with this approach in fully identifying at the species level, so we employed long-read whole genome sequencing via the Nanopore platform to resolve the identifications of six of these isolates.Throughout this process, we identified severalA. veronii,A. hydrophila, andA. dhakensisisolates. From our assessments,A. veroniiwas the most common isolate sequenced, and it was challenging to locate A hydrophila isolates, as many archived turned out to be differentAeromonasspp. when typed. The team generated growth curves for six isolates to optimize inoculum doses and tie optical density values to CFU/mL. Growth assessments were also performed using siderophores (DFO and DPD) to chelate iron in the culture media to potentially enhance virulence. Using this approach, we found that 2'2,-Bipyridyl (DPD) produced desired inhibition levels when compared with deferoxamine mesylate (DFO).When grown in large- and small-scale culture volumes with DPD, theAeromonasspp. isolate growth was inhibited when compared to non-siderophore growth trials.A 200uM concentration of DPD was identified as the optimal siderophore concentration for this pilot work.We performed 14 virulence screenings using LMB in sizes ranging from 5-50 g. Thein vivoscreenings involved immersion and IP-injection protocols in replicated tanks to discern isolate virulence. From our project plan, we did not find success in the mucus scrape immersion challenges (mortality rates <5%), so we employed the soft dorsal fin-clip model and found that we could achieve low-level mortality with several of the isolates.The CPM of the virulence assessments for immersion ranged from 3-14% CPM via immersion and 67-97% via IP injection. We selected twoAeromonasspp. isolates, ARS-LMB-32-2018 (A. veronii) and ARS-LMB-2022-09 (A. hydrophila), to advance into bacterin design and use in long-term trials. From the virulence assessments, ARS-LMB-32-2018 showed CPM of 14% via immersion (CFU/mL=1.85 x 107) and 97% via IP-injection (CFU/mL=1.49 x 107). These routes were also tested alongside DPD siderophore-cultured inocula, and we found no differences in CPM for both immersion and injection compared to the non-DPD cultured inocula. The ARS-LMB-2022-09 showed CPM of 3% via immersion (CFU/mL=2.16x 107) and 97% via IP-injection (CFU/mL=8.25 x 106). Again, the DPD addition did not enhance isolate virulence for both challenge routes.

Publications

  • Type: Conference Papers and Presentations Status: Published Year Published: 2024 Citation: Ledford OP, Schneider CM, LaFrentz BR, Garc�a JC, Butts IAE, Bruce TJ (2024) Challenge model development for Aeromonas spp. infection in juvenile Micropterus salmoides, Annual Meeting of the American Fisheries Society Fish Health Section & 63rd Western Fish Disease Workshop, July 30-August 2, Boise, ID, USA.