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Cycle 4 (2015 Deadline)
Monitoring the disturbance of the microbiota in Amazonian soils during conversion of forest to pasture and its consequences on cattle health
PI: Ederson Jesus (ederson.jesus@embrapa.br), Embrapa (Brazilian Corporation of Agricultural Research)
U.S. Partner: James Cole, Michigan State University
Project Dates: October 2015 - September 2021
Project Overview
 | | Dr. Jesus (left) with U.S. partner Dr. James Cole of Michigan State University and Dr. Kostas Konstantinidis from Georgia Tech, along with a third U.S. partner, Dr. Adina Howe of Iowa State University at the MiGA workshop (photo courtesy of Dr. Jesus). |
Pandemics of “swollen face,” a bacterial-origin periodontitis disease afflicting ruminant livestock, have been correlated with deforested areas in Brazil (Döbereiner et al., 2000). This disease, which is also known as "lumpy face," was commonly reported in Brazil during the 1960s and 1980s. New cases have recently been observed in sheep and goat flocks in the Amazon, under the same epidemiological conditions and with the same characteristics observed in bovines. In such circumstances, the disease has destroyed herds of livestock, often up to 90% of the animals. Dr. Jesus and his project collaborators hypothesize a link between the “swollen face” disease and shifts in the soil microbial communities as a consequence of deforestation and pasture introduction. This belief is based on previous evidence showing that this disease is triggered by deforestation, which in turn leads to significant changes in the soil communities, favoring specific populations such as actinomycetes. The team’s Phase I objective is to characterize correlations between the soil environment, changes in the microbial community due to deforestation, and the occurrence of this disease. Once more specific correlations are identified, in Phase II of the project they will experimentally test hypotheses (e.g., causation) generated through isolating key microbes and using culture-dependent and independent techniques. Answering these questions is important to advance towards a cure for the disease and design monitoring methods and alternative management to reduce its incidence. Additionally, confirming the link between the occurrence of diseases, deforestation, and changes in biodiversity will contribute to the delineation of policies to hinder deforestation and to promote biodiversity conservation. As part of the effort, the U.S. Government-supported partner, Dr. James Cole, will provide training and support with bioinformatic analysis of the datasets, sharing analytical tools he uses in his own research.
The world’s growing population and their increasing demand for animal protein raises concerns over the pressure for the creation of new pastures to meet this demand, especially in countries like Brazil, which is the world’s leading beef exporter. New pastures are created at the expense of native lands, including the Brazilian Amazon. In fact, pasture introduction is the major driver of deforestation in the region, and alternatives to reduce this pressure are needed. Within this context, this project can contribute with information to support policymakers in their decisions, as well as to create alternatives to the sustainable management of pre-existing pasture lands. The results of this project may also contribute to designing sustainable, innovative management systems, such as the integrated crop-livestock-forest system, which has been recognized by FAO, the Ministry of Agriculture of Brazil, and Embrapa as an alternative to stimulate the use of pre-existing pasture lands, guarantee food and agricultural security, and discourage the deforestation of new areas for agriculture and livestock production.
Final Summary of Project Activities
This project concluded at the end of September 2021 after six years of dedicated efforts by the PI Dr. Ederson Jesus and his colleagues. Dr. Jesus reports that they achieved all their Phase I objectives on the project, including (1) carrying out a prospecting survey of livestock swollen face disease in regions threatened by deforestation; (2) characterizing the pasture systems; and (3) applying multivariate methods to identify variables correlated with occurrence of the disease. All field collection and DNA sequencing activities were completed, and although the project has ended, the researchers continue to prepare additional manuscripts and student dissertations. Members of all three subgroups working on the project (Embrapa Agrobiologia, Embrapa Solos, and UNESP) have integrated their data, drawn some conclusions about some of the patterns found, and raised new hypotheses to be tested in the future. Regarding Phase II on the project, the researchers concluded the field experiment and laboratory activities. Co-PI Dr. Iveraldo Dutra and his team did a careful evaluation of animal health and sampled soil and grasses during the field experiment in Araçatuba. They finished DNA extraction from the soil and animal samples and expect to have sequence data to analyze in early 2022.
Several expeditions were carried out during the project, including five trips for soil characterization and microbiological sampling in five municipalities. Soil physical, chemical, and microbiological attributes were measured for at least 92 sampling points, which also included the examination of litter bacterial communities in the forest. Fifteen soil profiles were examined, providing a comprehensive survey of soils in the studied farms. More expeditions were carried out for veterinary work, including 14 expeditions to farms and four slaughterhouses in eight municipalities in the Amazon region. A total of 334 animals were examined on rural properties, and samples of subgingival biofilm from 54 animals and ruminal fluid from 22 animals were collected. These samples were sent for 16S rRNA gene sequencing and the results evaluated by bioinformatics analysis.
The prevalence of periodontal lesions in cattle in the evaluated areas ranged from 10.4% to 71.4%. These results show that periodontal diseases are common in cattle herds, but their occurrence is still neglected. The publication of these data will help to show that periodontal diseases are an extremely relevant health problem for livestock. The sequencing results show that there are differences in the composition between the dental microbiomes of healthy and sick animals, both for cattle, sheep, and goats. These results will contribute to the identification of potential pathogens and will help in the development of control and prevention measures for periodontal diseases in ruminants.
Regarding the relationship between the soil environment, microbiota, and animals, as reported in the previous sections, Dr. Jesus and his colleagues were able to identify soil, microbiological, and forage variables linked to a higher incidence of periodontitis. The results give support to a multifactorial relationship with the environment, with changes also observed at the level of microbial communities. As previously mentioned, their preliminary assumption is that the highest alpha and gamma diversities associated to a greater number of modularity classes in network analysis, indicates that the microbiota of high-severity level (HSL) pastures are reflecting intense environmental stress, characterizing its dysbiosis. This is a hypothesis that should be tested in the future, and the researchers expect to confirm it in their analysis of sequencing data coming from Phase II. The hypothesis that Actinobacteria may be involved was also supported by their higher abundance and the higher abundance of Streptomycin synthesis genes in HSL pastures. Based on these results, the team identified potential factors related to the incidence of the disease. The results point to new hypotheses that will help advance the comprehension of the interaction between the soil environment and the periodontal disease. Now that the researchers finally have results that can help in understanding the link between periodontal disease in cattle and their environment, these results will be important to guide future studies aiming at improving management practices to reduce the impacts of the disease. Dr. Dutra’s team has made significant progress in understanding the microbiome related to the disease itself, and that will contribute to the identification of potential pathogens and help in developing control and prevention measures.
Although the PEER project has ended and his primary U.S. partner Dr. James Cole has retired, Dr. Jesus will be continuing to collaborate with U.S. co-partner Dr. Adina Howe of Iowa State University. In fiscal year 2022, he has been awarded a Joint Genome Institute Community Science Program Annual Grant, funded by the U.S. Department of Energy, to sequence soil metagenomes from forest and pasture soils with a focus on environmental sustainability: https://jgi.doe.gov/our-projects/csp-plans/approved-proposals-fy22/ The major goal is to study the role of microbial communities from soil organic layers of the forest and pasture in nutrient cycling. The project will be carried out in collaboration with Dr. Howe, and the JGI award will pay all sequencing costs and give support with data analysis (an estimated value for these services is approximately US $100,000). Dr. Jesus and his colleagues will sequence 3 Tb of data for 60 metagenomes.
Dr. Dutra’s team has established a scientific partnership with a group of researchers from the United Kingdom (University of Glasgow) and Netherlands (University of Amsterdam) established since 2015. These researchers contributed with data analysis and bioinformatics analysis. We have established contact and intend to expand this partnership with researchers from other universities (University of Liverpool and University of Surrey) since we intend to develop an epidemiological study about dental diseases in the United Kingdom. Dr. Dutra’s group recently established a connection with researchers from Portugal (University of Évora) with the aim of working to define how diet contributes to the development of periodontal diseases. The researchers are also in contact with ASTRE (Animal, Santé, Territoires, Risques et Ecosystemes), a research unit in Montpellier, France, devoted to the study of the relationships between health and the environment. They remain eager to establish new contacts with other research institutions looking to establish collaborations and develop new projects to advance their findings.
Publications
Borsanelli, A.C., F.R.F. Athayde, S.D. Agostinho, M.P. Riggio, and I.S. Dutra. 2021. Dental biofilm and its ecological interrelationships in ovine periodontitis. Journal of Medical Microbiology 70:7. https://doi.org/10.1099/jmm.0.001396
Rocha, F.I., T.G. Ribeiro, M.A. Fontes, S. Schwab, M.R.R. Coelho, J.F. Lumbreras, P.E.F. da Motta, W.G. Teixeira, J. Cole, A.C. Borsanelli, I.S. Dutra, A. Howe, A.P. Oliveira, and E.C. Jesus. 2021. Land-use system and forest floor explain prokaryotic metacommunity structuring and spatial turnover in Amazon forest-to-forest conversion areas. Frontiers in Microbiology, 12, 657508. https://doi.org/10.3389/fmicb.2021.657508
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