Source: UNIVERSITY OF KENTUCKY submitted to
TOO HOT TO HANDLE: HOW WILL THE CHANGING CLIMATE AFFECT HERITABLE SYMBIONTS OF A GENERALIST PREDATOR GUILD?
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
NEW
Funding Source
Reporting Frequency
Annual
Accession No.
1029974
Grant No.
2023-67012-39352
Project No.
KY0Doremus01
Proposal No.
2022-09639
Multistate No.
(N/A)
Program Code
A1112
Project Start Date
Apr 1, 2023
Project End Date
Mar 31, 2025
Grant Year
2023
Project Director
Doremus, M. R.
Recipient Organization
UNIVERSITY OF KENTUCKY
500 S LIMESTONE 109 KINKEAD HALL
LEXINGTON,KY 40526-0001
Performing Department
(N/A)
Non Technical Summary
Arthropods play major roles in agricultural production by acting as biological control agents or crop pests. Most arthropods also host maternally inherited, intracellular bacterial symbionts that can provide their host with required nutrients, protect hosts from important natural enemies, or manipulate the outcomes of host reproduction. High temperatures can destabilize these symbioses by reducing transmission efficacy and preventing the symbiont from modifying their host. The predicted increase in global temperatures has unclear consequences for heritable symbionts and their arthropod hosts. Spiders are an important but understudied group of generalist predators that often harbor complex heritable symbiont communities and are emerging models for studying heritable symbionts. This project will use field surveys, laboratory-based experiments exposing spiders to current and predicted high temperatures, and genomic analyses to address three questions: 1) Does climate shape symbiont frequency in US spider populations? 2) Does temperature stress destabilize heritable symbioses? 3) Do symbiont genomes encode responses to temperature stress? Results will reveal how climate influences spider symbionts and will establish a new spider model system for studying heritable symbioses. This research will further characterize the role of symbionts in arthropod biology and how climate change might affect these widespread symbioses. Data from this project will be made publicly available for potential use in other research, including developing models predicting the impact of climate change on arthropod populations and their heritable symbionts. This project will also generate a highly trained and competitive workforce that are well prepared to address emerging agricultural challenges, including agricultural climate adaptation, by providing postdoctoral and undergraduate research, mentorship, teaching, and project management training. It will also increase scientific literacy in the general public by developing an educational module on DNA sequencing for undergraduate and high school students. This module will include hands on experience extracting DNA and analyzing DNA sequencing, common technique employed by biology labs.
Animal Health Component
0%
Research Effort Categories
Basic
100%
Applied
0%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2113120113060%
2110430107020%
2114010106020%
Goals / Objectives
The major goals for this project are to:Research how climate and temperature stress affect heritable symbioses between arthropods (linyphiid spiders) and their intracellular, bacterial symbionts. It will use the emerging spider model Mermessus fradeorum and establish lab cultures ofa second spider system to serve as a new model for spider-microbesymbiosis research.Determine how temperature stress affects the stability of linyphiid heritable symbiont communities, including how high temperatures affect symbiont-induced manipulation of arthropod reproduction.Determine whether climate shapes heritable symbiontcommunities in natural populations of linyphiid spiders in US alfalfa fieldsSequence and analyze the genomes of the M. fradeorum symbiont community and the community of a second novel spider model. Genomes will be used to identify canidate symbiont effectors involved in manipulating host reproduction and the symbiont thermal stress response.Establish an interactive educational module for undergraduate and high school students on DNA sequencing and COI barcoding.Provide training in project management, mentorship, bioinformatics techniques, and networking opportunities for PD Doremus to facilitate his transition to a research-focused faculty position.Provide training in molecular research techniques for two undergraduate researchers
Project Methods
We will survey natural linyphiid populations from alfalfa fields in 8 states across two climatic zones representing a "cool" and "warm" climate. Spider collection metadata will be recorded and spiders will undergo DNA extraction and COI barcoding to identify spider species. We will characterize the microbiome of the 4-5 most prevalent spider species using 16S rRNA sequencing to identify bacterial symbionts, focusing primarily on heritable symbionts. I will analyze symbiont occurrance for each spider species using generalized linear models incorporating vegetation status, locality, and climatic variables. We will establish a lab culture for one of these spider species for use in downstream experiments testing the effect of temperature stress on symbiont transmission.We will next use laboratory based experiments with the linyphiid M. fradeorum to measure the effect of temperature stress on symbiont-induced cytoplasmic incompatibility (CI, a form of lethal reproductive sabotage of uninfected offspring) and feminization. Spiders will develop at either a cool control temperature at which the symbiosis is stable or an elevated temperature representing current high temperatures experienced by M. fradeorum in Kentucky. Following temperature exposure, spiders will be used in experimental crosses to measure the symbiont-induced phenotypes(sex ratio for feminization experiments, hatch rate for CI). All spiders will be stored in 95% EtOH for DNA extraction and symbiont infection confirmation using PCR and symbiont density estimation following temperature exposure using quanititative PCR. Experiments will be replicated using high temperatures reflecting predicted high temperatures experienced by spiders by the end of the century. Symbiont transmission rates (from mother to offspring) will be recorded following temperature exposure for M. fradeorum and thesecond linyphiid spider. Sex ratio and hatch rates will be analyzed using logistic regression, while symbiont density will be analyzed using ANOVAs, and transmission rate will be analyzed using Fisher's exact tests.Genomes for M. fradeorum symbionts and the symbionts of the newly established spider culture will be sequenced using a combination of Illumina short reads and PacBio long reads to resolved repetitive regions in the genome. Genomes will be assembled, circularized, quality checked, and rotated to the origin of replication using UniCycler. Genomes will be annotated using the NCBI Prokaryote Genome Annotation Pipeline, PLSDB (for plasmid annotation), and PHASTER (phage annotation). I will identify homologs of classical temperature stress proteins and chaperonins using TBLASTN and HMMer and will compare the number of intact or psuedogenized temperature shock genes with the symbiont's temperature sensitivity as determined by the previous lab experiments. I will next test if putativetemperature stress response genes are expressed following temperature shock. Spiders exposed to either high temperatures or cool control temperatures will be flash frozen in liquid nitrogen prior to having their RNA extracted. Using reverse transcriptase qPCR, I will estimate the expression of putative symbiont temperature shock genes relative to a housekeeping gene. Gene expression will be analyzed using ANOVAs. I will use similar methods to also identify putative effectors involved in symbiont-induced CI and feminization, using TBLASTN and HMMer to search for effectors homologous to other known manipulative effectors, as well as genes encoding predicted eukaryotic interaction domains like ankyrins.Beyond research, this project will fund the development of two educational courses/modules. The first is a graduate level course on insect-microbe symbioses co-taught by PD Doremus and Mentor White. PD Doremus will be responsible for course design and leading discussions. The second unit is an educational module on DNA sequencing and COI barcoding using local spiders. This module will initially be presented as a portion of Mentor White's General Entomology course. Students will collect and stored a local specimen of spider in 95% EtOH. During a class and lab period, PD Doremus will lead a discussion on the underlying principles of DNA sequencing, COI Baracoding, and their usage in biology. During this period, students will extract spider DNA. In a subsequent lab period, students will amplify the COI sequence from their spider DNA using PCR. PD Doremus will perform PCR clean ups and send samples to an offsite sequencing facility. Students will then analyze sequence chromatograms, then use popular platforms like NCBI or the Barcode of Life Database to identify their spider species. This unit can potentially be adapted for high school students. The ultimate goal for this module to provide students hands on experience with common biological research techniques and to build a database of local spider species for downstream use in research.We will primarily use publication of results in peer reviewed journals as the final evaluation for research aims. We will also preesnt research results at conferences for feedback from peers prior to publication. During the project, yearly updates will be provided to anadvisory committee composed of the co-mentors White and Dunning Hotopp, and well as our collaborator Yuval Gottlieb (Israel) on project progress. This committee will offer feedback on the progress towards major goals. PD Doremus will additionally meet with Mentor White on a weekly basis and mentor Dunning Hotopp on a monthly basis for project udpates and feedback.For mentorship goals, Mentor White will evaluate mentorship ofundergraduate students supervised by PD Doremus, meeting with them once in the midpoint of them first year and hosting a final evaluation at the end of their second year. Their feedback will be provided to PD Doremus so he can adjust mentorship accordly. Undergraduate reserach will also be evaluated via presentations at the Undergraduate Research Showcase at the University of Kentucky (UKY) each spring.For teaching goals, PD Doremus will incorporate pedagogical guidance and feedback from the Center for Enhancement of Learning and Teaching (CELT) at UKY during module and course development. Mentor White will also provide feedback on course design and teaching. Students will be provided with an opportunity to evaluate the course/module and PD Doremus' teaching at the end of the educational course. This feedback will be incorporated in subsequent iterations of the educational course.

Progress 04/01/23 to 03/31/24

Outputs
Target Audience:Presented research talks to a national and international audience of symbiosis and entomology researchers at three conferences. Conferences included the 4th ISF Research Workshop on Symbiosis hosted by the Hebrew University of Jerusalem, the 2023 Wolbachia meeting in Chania, Crete, and the Annual Entomological Society of Entomology conference in National Harbor, MD. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? PD Doremus has received experience mentoring a research team of undergraduates, as well as networking opportunites via his attendence at three research conferences. PD Doremus has also begun interviewing for faculty positions. Two undergraduate researchers have received training in molecular research techniques. One of these students performed her own study (a portion of the experiments testing how temperature affects feminization) and presented her work at the 2023 Entomology Society of America (ESA) conference. Her talk was awarded 2nd place in her section of undergraduate research talks. How have the results been disseminated to communities of interest?Research on the effects of temperature on M. fradeorum feminization, as well as the role of Wolbachia in this manipulation have been presented as research talks at ESA in National Harbor, Maryland, as well as at the 2023 Wolbachia conference in Chania, Crete. The Wolbachia conference is a well-attended meeting focusing on heritable symbioses that draws research from across the world. What do you plan to do during the next reporting period to accomplish the goals? Complete the first run of 16S rRNA sequencing and analysis ofmicrobiomes of linyphiids collectedin 2023. Based on the results of this initial run, we will target several sites to collect additional samples of certain species. Samples collected in 2024 will undergo processing, species identification, and microbiome sequencing. This second collection period will also yield additional spider species to start lab cultures. Perform experiments estimating effect of temperature and symbiont coinfection on symbiont titer Write and make publically available a manuscript of the effects of temperature on symbiont-induced feminization in M. fradeorum Write and make publically available a manuscript detailing the role of Wolbachia and coinfection in causing feminization. Extract high molecular weight symbiont DNA for PacBio long-read sequencing and begin construction and analysis of the M. fradeorum symbiont genomes Present research at the 2024 ESA conference in Phoenix, AZ

Impacts
What was accomplished under these goals? Using several lab-based experiments exposing M. fradeorum to different temperature regimens, we found that warm temperatures representative of current summertime high temperatures in Kentucky reduce the effectiveness of two symbiont-induced forms of reproductive manipulation. Warm temperatures may influence the symbiont infection dynamics and host biology of the M. fradeorum system. One of these manipulations is the symbiont-induced feminization of male hosts, which resultsin a phenotypic female capable of vertically transmitting the symbiont to their offspring. Spider development at warm temperatures caused a delayed, trans-generational failure of feminization in their offspring resulting in a restoration of male production. This feminization failure was associated with a shift in the spider symbiont community caused by the vertical transmission failure of several symbionts from mother to offspring. This indicatesthat one or more of the affected bacteria are responsible for feminization. The feminization phenotype is restored following additional spider generations raised at cooler temperatures, suggesting that this phenotype may have variable efficacy throughout the growing season. This variable efficacy, combined with inefficient transmission rates, may be responsible for the lower infection rates for the feminizing symbionts. These temperature studies also revealed that the five symbionts infectingM. fradeorum vary in their thermal tolerance. Rickettsiella appears to be the most thermally robust symbiont, with stable transmission across multiple generations at warm temperatures. The three Wolbachia strains show intermediate tolerance and are variably lost following multiple generations at warm temperatures. Tisiphia is extremely temperature sensitive, exhibiting total transmission failure following initial exposure to warm temperatures. Using crossing assays with a number of differentially infected spider lines, we have identified one strain of Wolbachia as the causitive agent of feminization, although coinfection with multiple symbionts increases feminization efficacy. This synergystic effect may promote the persistance ofquintuple infections in host populations. To begin characterizing how climate shapes heritable symbiont communities of linyphiids, we have collected ~1000 spiders from 17 sites across 13 states representing a latitudinal gradient. Spiders are currently undergoing intial processing to identify species using a combination of morphology and CO1 sequencing. We are currently preparing a high-throughput sequencing run of the 16S rRNA gene to characterize the microbiome of a subset of these samples.

Publications