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UT Professors Investigate Solutions for “Forever Chemicals”

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University of Tennessee, Knoxville faculty members Shawn Campagna, professor and associate department head in chemistry, and Frank Loeffler, Governor’s Chair professor in microbiology, have made a discovery that could lead to new capabilities for managing environmental contamination.

Commercially used per- and polyfluoroalkyl substances (PFAS) were developed in the 1940’s and made their way into a variety of common household products. Today, PFAS are used for plastic and rubber manufacturing and in food wrappers, umbrellas, firefighting foam and more.

PFAS have also been called “forever chemicals” due to their resistance to breaking down in both the environment and the human body. PFAS have been discovered lingering in rivers, Arctic sea ice, human breast milk and in the blood of 97% of Americans. Most troublesome is their potential impact on human health and PFAS have been linked to metabolic disruption, obesity, diabetes, immune suppression, and cancer.

Loeffler and Campagna’s work, recently published in Environmental Science and Technology, explores a potential avenue for decreasing broad contamination with these chemicals. Their team found that a naturally occurring soil bacterium, Pseudomonas sp. strain 273, was capable of degrading and detoxifying 1,10-difluorodecane, a fluorinated compound that could be a model for dealing with PFAS. Surprisingly, this bacterium was also able to use the fluorine containing byproducts to build lipid bilayers, or cellular membranes, which indicates that we don’t yet know all that we should about the fate of this type of compounds in biological systems.

“This research is important since fluorinated organic chemicals are emerging contaminants, and we do not yet know how and if they enter the food web,” said Campagna. “The fact that bacteria can incorporate breakdown products of these molecules into their biomass indicates that we don’t fully understand the environmental impact of these contaminants.”

This discovery developed from a long-standing series of collaborations between Campagna and Loeffler and leverages the capabilities of both the Center for Environmental Biotechnology and the Biological and Small Molecule Mass Spectrometry Core.

“There is a pressing need to demonstrate that natural degradation processes for PFAS exist – that they are not forever chemicals,” said Loeffler. “The new findings emerged through collaborative efforts at the interface of disciplines, specifically environmental microbiology and analytical chemistry. My group obtained and characterized the unique microorganism, and Dr. Campagna’s group had the instrumentation and expertise to perform the analytical procedures. The results are a product of teamwork and neither group individually would have succeeded.”

Campagna and Loeffler hope their work can lead to further discoveries of bacteria capable of degrading the entire range of fluorinated pollutants, which could lead to removing PFAS from contaminated areas like drinking water.

As part of the bipartisan infrastructure law funding initiative, the U.S. Environmental Protection Agency is making available $1 billion in grant funding, the first of $5 billion through the law. This initiative aims at reducing PFAS in drinking water specifically in communities facing disproportionate impacts.

Both Loeffler and Campagna have been contacted by the Tennessee Department of Environment and Conservation (TDEC) regarding state mandated PFAS monitoring in drinking water. Their capabilities are facilitating statewide efforts to improve the quality of life for all residents of the state of Tennessee.

Campagna Lab published in Frontiers In Microbiology

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The Campagna lab published their work “Comparative Decomposition of Humans and Pigs: Soil Biogeochemistry, Microbial Activity and Metabolomic Profiles” in Frontiers In Microbiology.

Vertebrate decomposition processes have important ecological implications and, in the case of human decomposition, forensic applications. Animals, especially domestic pigs (Sus scrofa), are frequently used as human analogs in forensic decomposition studies. However, recent research shows that humans and pigs do not necessarily decompose in the same manner, with differences in decomposition rates, patterns, and scavenging.

The objective of this study was to extend these observations and determine if human and pig decomposition in terrestrial settings have different local impacts on soil biogeochemistry and microbial activity. In two seasonal trials (summer and winter), we simultaneously placed replicate human donors and pig carcasses on the soil surface and allowed them to decompose. In both human and pig decomposition-impacted soils, they observed elevated microbial respiration, protease activity, and ammonium, indicative of enhanced microbial ammonification and limited nitrification in soil during soft tissue decomposition. Soil respiration was comparable between summer and winter, indicating similar microbial activity; however, the magnitude of the pulse of decomposition products was greater in the summer.

Using untargeted metabolomics and lipidomics approaches, they identified 38 metabolites and 54 lipids that were elevated in both human and pig decomposition-impacted soils. The most frequently detected metabolites were anthranilate, creatine, 5-hydroxyindoleacetic acid, taurine, xanthine, N-acetylglutamine, acetyllysine, and sedoheptulose 1/7-phosphate; the most frequently detected lipids were phosphatidylethanolamine and monogalactosyldiacylglycerol. Decomposition soils were also significantly enriched in metabolites belonging to amino acid metabolic pathways and the TCA cycle.

Comparing humans and pigs, they noted several differences in soil biogeochemical responses. Soils under humans decreased in pH as decomposition progressed, while under pigs, soil pH increased. Additionally, under pigs we observed significantly higher ammonium and protease activities compared to humans. We identified several metabolites that were elevated in human decomposition soil compared to pig decomposition soil, including 2-oxo-4-methylthiobutanoate, sn-glycerol 3-phosphate, and tryptophan, suggesting different decomposition chemistries and timing between the two species.

Together, this work shows that human and pig decomposition differ in terms of their impacts on soil biogeochemistry and microbial decomposer activities, adding to our understanding of decomposition ecology and informing the use of non-human models in forensic research.

The group also published their work “Enterococcus faecalis Readily Adapts Membrane Phospholipid Composition to Environmental and Genetic Perturbation” in Frontiers In Microbiology. 

The bacterial lipid membrane, consisting both of fatty acid (acyl) tails and polar head groups, responds to changing conditions through alteration of either the acyl tails and/or head groups. This plasticity is critical for cell survival as it allows maintenance of both the protective nature of the membrane as well as functioning membrane protein complexes. Bacteria that live in fatty-acid rich environments, such as those found in the human host, can exploit host fatty acids to synthesize their own membranes, in turn, altering their physiology. Enterococcus faecalis is such an organism: it is a commensal of the mammalian intestine where it is exposed to fatty-acid rich bile, as well as a major cause of hospital infections during which it is exposed to fatty acid containing-serum. Within, the group employed an untargeted approach to detect the most common phospholipid species of E. faecalis OG1RF via ultra-high performance liquid chromatography high-resolution mass spectrometry (UHPLC-HRMS).

The group examined not only how the composition responds upon exposure to host fatty acids but also how deletion of genes predicted to synthesize major polar head groups impact lipid composition. Regardless of genetic background and differing basal lipid composition, all strains were able to alter their lipid composition upon exposure to individual host fatty acids. Specific gene deletion strains, however, had altered survival to membrane damaging agents. Combined, the enterococcal lipidome is highly resilient in response to both genetic and environmental perturbation, likely contributing to stress survival.

Campagna Lab Published in JNP

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The Campagna Lab published their work “Isoflurane anesthesia disrupts the cortical metabolome” in a collaborative piece in the Journal of Neurophysiology (JNP). 

Identifying similarities and differences in the brain metabolome during different states of consciousness has broad relevance for neuroscience and state-dependent autonomic function. This study focused on prefrontal cortex (PFC) as a brain region known to modulate states of consciousness.

Anesthesia was used as a tool to eliminate wakefulness. Untargeted metabolomic analyses were performed on microdialysis samples obtained from mouse PFC during wakefulness and during isoflurane anesthesia.

Analyses detected 2153 molecules, 91 of which could be identified. Analytes were grouped as detected during both wakefulness and anesthesia (n=61), and as unique to wakefulness (n=23) or anesthesia (n=7). Data were analyzed using univariate and multivariate approaches. Relative to wakefulness, during anesthesia there was a significant (q < 0.0001) four-fold change in 21 metabolites. During anesthesia 11 of these 21 molecules decreased and 10 increased.

The Kyoto Encyclopedia of Genes and Genomes database was used to relate behavioral state specific changes in the metabolome to metabolic pathways. Relative to wakefulness, most of the amino acids and analogs measured were significantly decreased during isoflurane anesthesia. Nucleosides and analogs were significantly increased during anesthesia. Molecules associated with carbohydrate metabolism, maintenance of lipid membranes, and normal cell functions were significantly decreased during anesthesia.

Significant state-specific changes also were discovered among molecules comprising lipids and fatty acids, monosaccharides, and organic acids. Considered together, these molecules regulate point to point transmission, volume conduction, and cellular metabolism. The results identify a novel ensemble of candidate molecules in PFC as putative modulators of wakefulness and the loss of wakefulness.

Campagna Gives Talk for Harvard’s MSI Seminar Series

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The Microbial Sciences Initiative (MSI) at Harvard University is an interdisciplinary science program aimed at a comprehensive understanding of the richest biological reservoir of the planet, the microbial world.

Shawn Campagna presented a talk for this series titled “Using Metabolomics to Understand the Function of Environmentally Relevant Microbial Consortia.”

 

ORI Names Campagna Interim Director of Strategic Programs

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President Randy Boyd shared some developments at the Oak Ridge Institute at UT (ORI at UT). A national search for the first executive director and vice provost of the Oak Ridge Institute at UT is underway.

Shawn Campagna
Shawn Campagna

ORNL Director Thomas Zacharia and Randy Boyd, in consultation with UT Knoxville Chancellor Donde Plowman and UT Health Science Center Chancellor Steve Schwab, have named Michelle Buchanan, ORNL deputy for science and technology, and Stacey Patterson, UT System vice president for research, as interim co-directors of ORI at UT until a director is named. Suresh Babu, a UT-ORNL Governor’s Chair for Advanced Manufacturing and Bredesen Center Director, will serve as ORI at UT’s interim education director. Shawn Campagna, UT Knoxville associate department head of chemistry and Director of Science Alliance, will serve as the interim director of strategic programs. Jean Mercer, UT Knoxville assistant vice chancellor for research and director of the office of sponsored programs, will serve as interim director of operations.