Source: CARY INSTITUTE OF ECOSYSTEM STUDIES submitted to
HOW AGRICULTURAL ANTIBIOTICS AND MANURE INTERACT TO SHAPE SOIL COMMUNITIES, ECOSYSTEM FUNCTION AND ENVIRONMENTAL ANTIBIOTIC RESISTANCE
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1028322
Grant No.
2020-67012-36587
Cumulative Award Amt.
$88,271.35
Proposal No.
2021-12747
Multistate No.
(N/A)
Project Start Date
Sep 1, 2021
Project End Date
Jun 30, 2023
Grant Year
2022
Program Code
[A7201]- AFRI Post Doctoral Fellowships
Project Director
Lucas, J.
Recipient Organization
CARY INSTITUTE OF ECOSYSTEM STUDIES
280 L Sharon Turnpike Box AB
MILLBROOK,NY 12545-0129
Performing Department
(N/A)
Non Technical Summary
Antibiotic compounds are frequently used to promote the health and growth of livestock. As with many medicines, the un-metabolized, active compounds are eliminated through animal waste products and introduced to the surrounding environment. How these compounds affect soil food webs is poorly resolved. This proposed project aims to understand how a commonly administered livestock antibiotic interacts with manure to shape soil communities, ecosystem function and antibiotic resistance. Using antibiotic-laden manure from dairy cattle, I will conduct a field experiment to assess how antibiotic compounds affect soil ecosystems and their function. I hypothesize that antibiotics change the microbial community in manure and agricultural soils, slowing decomposition rates. Furthermore, I hypothesize that the addition of antibiotics creates a metabolically stressful environment for microbiota, increasing their production of greenhouse gases and the prevalence of antibiotic resistant genes. Finally, I hypothesize that antibiotic-laden manure decreases invertebrate diversity and abundance by lowering microbial biomass and via deleterious effects on invertebrate microbiome. Through field experiments, invertebrate collections, and microbial analysis, I will assess how the introduction of antibiotic-laden manure disrupts the soil food web community and the ecosystem services it provides. The results of this study will help shape future agricultural practices, while providing insight into what governs the health of economically important agricultural pasturelands. The proposed project addresses the AFRI priority areas of Bioenergy, Natural Resources and Environment; Animal health and production and animal products; and Agriculture Systems and Technology. This project will help develop the research, education, and mentorship credentials of the Project Director.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
0%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
1020110107050%
3070110106020%
2110110107030%
Goals / Objectives
This project explores how antibiotics present in livestock waste influence microbial and invertebrate communities. We predict that the introduction of these biologically active products can disrupt the natural function and health of agricultural ecosystems. Through the disruption of natural microbial communities, the ability for soils to retain and recycling importantnutrients may be diminished. We also may find that carbon storage is reduced due to the increased metabolic stress of microbial communities under antibiotic attack. Similarly, if antibiotics harm the native invertebrate community, we may find that soils have reduced rates of decomposition and lower moisture retention. The soil texture may also be disrupted through the removal of key ecosystem engineers like Annelida. This project will fill a critical gap in our knowledge of how both antibiotic compounds and manure inputs shape soil function, while also linking soil health to human health.Primary Objectives(1) Determine how antibiotic additions affect ecosystem function in agricultural soils(2) Examine how microbial and invertebrate communities respond to antibiotics(3) Assess how antibiotic additions influence antibiotic resistant gene abundance anddiversity
Project Methods
Work already accomplished:The field portion of the proposed project will be conducted at two paired locations (1) the remnant Palouse prairie research reserve at Paradise Ridge, ID at the University of Idaho's Moscow campus and (2) the University of Idaho's experimental Kambitsch Farm. These paired sites will allow me to examine whether historically managed fields respond differently from uncultivated grasslands.Manure will be collected and homogenized from 10 dairy cattle at the University of Idaho's Dairy Center. None of the cattle inour study will have received a previous course of antibiotics. I will then add our antibiotic to the manure, at a rate equal to the average excretion rate. I will use Monensin, a broad-spectrum antibiotic that blocks bacterial cell protein transport, as it is one of the most frequently used antibiotics in livestock management and has a high active-compound excretion rate. A subset of the initial manure collections, and the antibiotic-manure mixtures will be collected and kept at -80C to preserve DNA. Their microbial communities will be assessed alongside samples.I will create plots by placing PVC collars (20 cm in diameter, inserted 5 cm into the soil), with open tops to allow for aboveground invertebrates to colonize. I will sample soil from each collar to establish a "starting" microbial community. Due to the destructive nature of invertebrate sampling, we will create 4 additional starting plots and sample them to establish the local invertebrate community. Antibiotics and/or manure will be added to collars in a 2 x 2 factorial design with six replicate collars per treatment per location. Treatments will be supplied monthly for a period of 4 months. Throughout the 4 months, grass-house gas emissions, decomposition rates and soil microbial and invertebrate communities will be sampled.To examine the effects of antibiotics and manure on green-house gas emissions and decomposition, each PVC collar will contain two decomposition bags filled with pre-weighed local plant litter. Bags will be collected after 60 and 120 days, and decomposition rates will be determined by measuring the amount of mass loss compared to initial weights. Gas fluxes of CO2 will be measured in the field using a portable Licor LI-8100A CO2 Gas Analyzer with a 20-cm closed, dynamic survey chamber (Licor, Nebraska, USA) attached to the PVC collar, with previously developed protocols.Gas emissions will be taken at day 1, 2, 4, 8, 16, 32, 64, 94, 120. At day 60 and 20, we will take a subsample of soil (~10 g) to perform C-mineralization (i.e., bioavailable C) assays and microbial biomass assessments. Combined, these measurements will allow us to quantify rates of microbial efficiency, an essential metric for understanding soil health.Soil from each PVC collar plot will be sampled at 0, 1, 4, 8, and 16 days after monthly treatment to examine microbial communities. At the time of sampling, we will measure temperature, moisture level, and pH in each plot. We will sample microbes using Zymo Xpeditiontm Soil/Fecal DNA Miniprep kits and protocol. We will analyze microbial communities by Illumina© sequencing libraries generated by PCR amplification of 16S bacterial and ITS fungal sequences. All microbial sequences will be processed, cleaned and taxonomically assigned using the pipeline DADA2. Subsequent analysis will be done in R v. 3.5.2.Invertebrate communities in half of the PVC will be sampled at day 60 and the second half at day 120 via the Berlese method. Once the invertebrate communities are sorted, we will determine the dominant taxa present across treatments. We will examine changes in the microbiome of these dominant invertebrates by sampling them as described above after surface sterilizing the invertebrates with a bleach solution. All further microbial analysis will be the same as described above.To be finished:I will use an emerging sequence-capture technique to examine the influence of antibiotics and manure on levels of ARGs. Broadly, this technique, name ResCap, allows researchers to amplify specific genes of interest across samples. Unlike traditional methods, sequence-capture allows for all known ARGs (~70,000) to be examined in one sequencing event. Sequence-capture is preferable to whole metagenome sequencing (WMS) which is often costly and inefficient due to the large portions of genetic material that are not of interest (i.e., DNA synthesis genes, structural coding genes). This technique also provides real-time measurements of gene abundance, allowing us to assess genetic diversity and abundance levels in unison. While commonly used in human medicine, ResCap has yet to be applied to soil ecosystems. Our novel approach of this technique could shape how we assess genetic and functional diversity in our soilsystems.Using the DNA extracted from soil microbial and invertebrate communities as describe above, I will use NimbleGen's SeqCap EZ (Roche Nimblegen, Inc) kits, probes and protocol to conduct analysis of ARGs. The genes for this study willbe compiled using a combination of ARG databases. After cleaning, "captured" DNA will then proceed through an additional brief amplification (ligation mediated PCR) prior to being purified and quantified. The DNA libraries will be sequenced on an Illmina© HiSeq at Cornell University's Institute of Biotechnology. Sequence processing will be conducted, and we will use the ResCap database to predict ARGs. Subsequent statistical analysis will be done in Rand will include linear models to compare levels of gene abundance across treatments. We will also examine important correlations between environmental variables, microbial and invertebrate community identity and ARGs using network analyses.

Progress 09/01/21 to 06/30/23

Outputs
Target Audience: The target audience for this work pertains to multiple scientific fields including but not limited to: agriculture, ecology, microbiology, entomology, infectious disease, and soil and water resources. To date we have been able to interact with many individuals in these various fields through virtual conferences, in person local conferences, and outreach events. Specifically we have worked with entomologists, microbiologists and infectious disease specialists at the Univeristy of Idaho. We have worked with land owners, farmers and land conservancy groups across NY and CT. We have also worked with waste water specialists who have helped us develop our qPCR analysis of potential ARG and other pathogens in our soil samples. We were also able to present this information at Washington State University's SoilCon conference. This conference had a huge range of participants, from academic, governmental, industry and private groups. Many local and national farmers attended which is a key group that I hope to work with as this project develops. This was a stake holder demographic that we had specifically targeted, and are please that we were able to meet with a variety of individuals in the midst of the COVID-19 pandemic. We have also worked with individuals at the University's Dairy Cattle Center and at the University of Connecticut that have been able to provide stakeholder input and have been essential in providing manure for the proposed project. This group has provided key insight into the farmer's perspective on how cattle are raised and have allowed us to ensure that the manure in this project is similar to other animals being raised in the area. Finally, we have provided guest lectures to a variety of lab meetings and in microbial ecology courses that were able to expose early career scientists to the work we are conducting. This is also a potential avenue for us to recruit future lab technicians and interested undergraduates. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? Although some initial professional development plans were interrupted by the onset of COVID-19, I have still had the opportunity to gain valuable experiences.One of the most rewarding and informative experiences has been working with our master's student technician, Dana. Through this project i have been able to support her on a part time basis. This has taught me how to manage both my time and hers, and has provided me with a lot of mentoring experience. We have developed multiple new protocols together and I have learned a lot about how to successfully delegate tasks.I have also been able to attend workshops during my time as a USDA postdoc. I am currently attending weekly microbial techniques workshops through the Ohio State University and weekly microbial science presentations through Arizona State University. These have been great learning opportunities, both from a technical standpoint and as an opportunity to see how far reaching microbial ecology is.Finally, I was also able to attend Soil Con at Washington State University. This week long conference brought "together" some of the brightest minds to discuss the topic of soil health from many viewpoints. Topics Included: State of Soil Health in Western US and Washington State Long-term Research Sites from Around the Globe Soil Health Indicators Soil Health in Specific Cropping System for Washington State How have the results been disseminated to communities of interest? The results of this study have been primarily presented to academic audiences. This has included one manuscript currently under review and multiple scientific presentations at Universities.However, I was also able to present this information at Washington State University's SoilCon conference. This conference had a huge range of participants, from academic, governmental, industry and private groups. Many local and national farmers attended which is a key group that I hope to work with as this project develops. Finally, I have been able to present a large portion of this work through soil health workshops. I have presented these to both farmer and general public audiences, and have done so online and in person. To date, I have provided this workshop to over 200 participants. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? I am pleased to report that the proposed work has been completed, and we have been able to expand on our initial study. Specifically, we have run a field experiment that explored nutrient cycling in preserved grasslands. This assessment of gas fluxes form this ecosystem has allowed us to link the introduction of antibiotic compounds to ecosystem function. We have found that the addition of antibiotics and manure consistently increases the amount of CO2 produced, but likely through different pathways. Antibiotics are likely causing microbial communities to become less efficient and therefore they are increasing their CO2 production. In contrast, manure additions also bring in a large and active new microbiome that is likely contributing to our observed raises in CO2 production. These results are currently under review for publication. We have also collected our soils after the field experiment and run them through a variety of assays. In order ot achieve our second objective, we have sequenced the bacterial and fungal communities for all of our field soils and found some distinct changes in the microbiomes depending on antibiotic and manure additions. We also extracted the invertebrate community from these soils to examine whether these different anthropogenic inputs are affecting the soil community. We have found interesting and complimentary results with the invertebrates. These communities decrease in the presence of antibiotics, but higher trophic orders increase. These results are also under review in a peer reviewed study. Finally, we combined qPCR approaches with a novel molecular technique called targeted gene capture to examine 80,000 antibiotic resistant genes at once. This will also allow us to develop a new pipeline for understanding soil molecular functions. The results of this work are under review, and a supplementary paper regarding our methods is currently being written.?

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2023 Citation: Wepking, C., J.M. Lucas, V.S. Boulos, M.S. Strickland. Antibiotic legacies shape the temperature response of soil microbial communities. Under Review, Soil Biology and Biogeochemistry
  • Type: Journal Articles Status: Under Review Year Published: 2023 Citation: J.M. Lucas and M.S. Strickland. Biogeographic patterns of antibiotic resistance in soil ecosystems. Under Review, PNAS
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2023 Citation: Lucas, J.M.* 2023. Rangeland carbon storage in the face of multiple global change factors. Society for Rangeland Management Meeting, Boise, ID.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2023 Citation: Lucas, J.M.* 2023. Stressed Out Soils: Understanding soil ecosystems in an era of Global Change. University of Illinois, Urbana-Champaign, IL.
  • Type: Conference Papers and Presentations Status: Other Year Published: 2022 Citation: Lucas, J.M. 2022. Understanding the biogeographic and environmental controls of antibiotic resistance in soils, Ecological Society of America Meeting, Montreal, Canada.


Progress 09/01/21 to 08/31/22

Outputs
Target Audience:The target audience for this work pertains to multiple scientific fields including but not limited to: agriculture, ecology, microbiology, entomology, infectious disease, and soil and water resources. To date we have been able to interact with many individuals in these various fields through virtual conferences, in person local conferences, internation conferences and outreach events. Specifically we have worked with entomologists, microbiologists, hydrologistsand infectious disease specialists at the Univeristy of Idaho, the University of Connecticut, Cornell Cooperative Extension and the Dutchess Land Conservancy in New York. We have also worked with waste water specialists who have helped us develop our qPCR analysis of potential ARG and other pathogens in our soil samples. We were also able to present this information at national and internation conferences. This allowed us to interact with scientists from a broad range of disciplines and locations. We were able to work with stakeholders by holding a soil health workshop during the summer of 2022. These local farmers and land owners came to Cary to learn about the research we are doing and learn how to understand and measuresoil health metrics. We are continuing to work with these farms to help implement soil health focused practices. We were able to help support an undergraduate REU this summer who has helped us further develop our work on antibiotic implications for the environment. Our research, Annemiek, had the opportunity to design her own project, implement it and present her work to a broad audience of scientists and the local community. Finally, we have provided guest lectures to a variety of lab meetings and in microbial ecology courses that were able to expose early career scientists to the work we are conducting. This is also a potential avenue for us to recruit future lab technicians and interested undergraduates. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Although some initial professional development plans were interrupted by the onset of COVID-19, I have still had the opportunity to gain valuable experiences. One of the most rewarding and informative experiences has been working with students and trainees throughout this project. Through this project I have been able to support two part time technicians and 2 undergraduate researchers.This has taught me how to manage both my time and theirs, and has provided me with a lot of mentoring experience. We have developed multiple new protocols together and I have learned a lot about how to successfully delegate tasks. I have also been able to attend workshops during this project. I am currently attending weekly microbial techniques workshops through the Ohio State University University and a science and policy workshop through AIBS. These have been great learning opportunities, both from a technical standpoint and as an opportunity to see how far reaching microbial ecology is. How have the results been disseminated to communities of interest?The results of this study have been primarily presented to academic audiences. This has included one manuscript currently under review and multiple scientific presentations at Universities. I was also able to attend the World Congress on Soil Science which allowed me to network and present to a large international audience. I was also able to present this information at Washington State University's SoilCon conference and at a soil health workshop that Ideveloped. Theconference had a huge range of participants, from academic, governmental, industry and private groups. Many local and national farmers attended which is a key group that I hope to work with as this project develops. What do you plan to do during the next reporting period to accomplish the goals?We are currently on track to finish up by June 2023. We are going to finalize our statistical analyses and then focus on writing up manuscripts. Wewill also continue to present our work at the Society for Rangeland Management conference and work with local stakeholders to develop additional workshops.

Impacts
What was accomplished under these goals? This report comes after the end of year 2of a 3year study. I am pleased to report that the entire field and much of the lab component of this study has been completed in this time. Specifically, primary objectives 1 and 2 have been almost completed. We have run a field experiment that explored nutrient cycling in preserved grasslands. This assessment of gas fluxes form this ecosystem has allowed us to link the introduction of antibiotic compounds to ecosystem function. We have found that the addition of antibiotics and manure consistently increases the amount of CO2 produced, but likely through different pathways. Antibiotics are likely causing microbial communities to become less efficient and therefore they are increasing their CO2 production. In contrast, manure additions also bring in a large and active new microbiome that is likely contributing to our observed raises in CO2 production. We have also collected our soils after the field experiment and run them through a variety of assays. In order ot achieve our second objective, we have sequenced the bacterial and fungal communities for all of our field soils and found some distinct changes in the microbiomes depending on antibiotic and manure additions. We also extracted the invertebrate community from these soils to examine whether these different anthropogenic inputs are affecting the soil community. We have finished up the invertebrate sort and are now finishing up a manuscript on these first two objectives. Finally, we are close to finishing ourthird objective. We are combining qPCR approaches with a novel molecular technique called targeted gene capture. The main focus of the second year of study will be to refine this novel technique in order to examine 80,000 antibiotic resistant genes at once. This will also allow us to develop a new pipeline for understanding soil molecular functions. The major focus at this time is to finish the final analyses and work on writing up the manuscripts. We may runa few more samples through traditional qPCR to serve as a control, but otherwise, we are fully on track to finish in June.

Publications

  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Lucas, J.M. 2022. Tiny things under our feet. Soil Ecology Society Meeting, Richland, WA.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Lucas, J.M. B. Sone , D. Whitmore, M. Strickland. 2022. Examining the influence of interacting global change factors on microbial communities and antibiotic resistance in soil ecosystems. Soil Ecology Society Meeting, Richland, WA
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Lucas, J.M. and M. Strickland. 2022. Anthropogenic and climatic stressors interact to disrupt soil communities and nutrient cycling. World Conference on Soil Science, Glasgow, Scotland.
  • Type: Conference Papers and Presentations Status: Accepted Year Published: 2022 Citation: Lucas, J.M. and M. Strickland. 2022. Understanding the biogeographic and environmental controls of antibiotic resistance in soils. Ecological Society of America Meeting, Montreal, Canada.
  • Type: Journal Articles Status: Under Review Year Published: 2022 Citation: Wepking, C., J.M. Lucas, V.S. Boulos, M.S. Strickland. Antibiotic legacies shape the temperature response of soil microbial communities.