Faculty Appointments
Assistant Professor of Biological Sciences
Assistant Professor of Pathology, Microbiology and ImmunologyAssistant Professor of Pathology, Microbiology and Immunology
Education
Ph.D., Genetics, University of Georgia, Athens, GeorgiaM.S., Biomedical Sciences, Auburn University, Auburn, AlabamaB.S., Molecular Biology, Auburn University, Auburn, Alabama
Research Description
Experimental Evolution and Population Genetics of Microbes.
Comprising most of the tree of life and constituting a major source of human disease, microbes are the most diverse organisms on earth. Armed with large population sizes and a multitude of ways to create sudden and dramatic changes to their genome, microbes are a fount of adaptive potential. Our research is focused on how
microbes adapt and diversify in novel complex environments. Among other environmental factors, these changes may be influenced by nutrient availability or limitation, spatial homogenization or structure, and the presence or absence of community members. We examine these questions on an individual (mutation accumulation), population (batch culture), and community (metagenomics) level.
Major topics that our lab investigates include:
Bacterial adaptation in response to fluctuating resources and stressful environments.
Effects of environment and microbial life history on genetic and epigenetic mutation rates.
Genetic drivers of stable subpopulation structure in experimentally evolving Escherichia coli populations.
Ecology and evolution of microbial interactions in the small intestine and urogenital microbiome.
For more information see our lab's website: http://www.behringerlab.wixsite.com/index
Comprising most of the tree of life and constituting a major source of human disease, microbes are the most diverse organisms on earth. Armed with large population sizes and a multitude of ways to create sudden and dramatic changes to their genome, microbes are a fount of adaptive potential. Our research is focused on how
microbes adapt and diversify in novel complex environments. Among other environmental factors, these changes may be influenced by nutrient availability or limitation, spatial homogenization or structure, and the presence or absence of community members. We examine these questions on an individual (mutation accumulation), population (batch culture), and community (metagenomics) level.
Major topics that our lab investigates include:
Bacterial adaptation in response to fluctuating resources and stressful environments.
Effects of environment and microbial life history on genetic and epigenetic mutation rates.
Genetic drivers of stable subpopulation structure in experimentally evolving Escherichia coli populations.
Ecology and evolution of microbial interactions in the small intestine and urogenital microbiome.
For more information see our lab's website: http://www.behringerlab.wixsite.com/index
Research Keywords
Evolution, Microbiology, Bacterial Genetics, Population Genetics, Genomics, epigenetics, epimutation, Microbiome, Urinary Tract, Stress resistance, Mutation
Publications
Behringer MG, Ho WC, Miller SF, Worthan SB, Cen Z, Stikeleather R, Lynch M. Trade-offs, trade-ups, and high mutational parallelism underlie microbial adaptation during extreme cycles of feast and famine. Curr Biol [print-electronic]. 2024 Apr 4/8/2024; 34(7): 1403-1413.e5-1413.e5. PMID: 38460514, PII: S0960-9822(24)00215-X, DOI: 10.1016/j.cub.2024.02.040, ISSN: 1879-0445.
Worthan SB, McCarthy RDP, Delaleau M, Stikeleather R, Bratton BP, Boudvillain M, Behringer MG. Evolution of pH-sensitive transcription termination during adaptation to repeated long-term starvation. BioRxiv. 2024 Mar 3/1/2024; PMID: 38464051, PMCID: PMC10925284, PII: 2024.03.01.582989, DOI: 10.1101/2024.03.01.582989.
Chuang YC, Haas NW, Pepin R, Behringer MG, Oda Y, LaSarre B, Harwood CS, McKinlay JB. Bacterial adenine cross-feeding stems from a purine salvage bottleneck. ISME J. 2024 Jan 1/8/2024; 18(1): PMID: 38452196, PMCID: PMC10976475, PII: 7624067, DOI: 10.1093/ismejo/wrae034, ISSN: 1751-7370.
Stone CJ, Boyer GF, Behringer MG. Differential adenine methylation analysis reveals increased variability in 6mA in the absence of methyl-directed mismatch repair. MBio [print-electronic]. 2023 Oct 10/31/2023; 14(5): e0128923. PMID: 37796009, PMCID: PMC10653831, DOI: 10.1128/mbio.01289-23, ISSN: 2150-7511.
Chuang YC, Haas NW, Pepin R, Behringer M, Oda Y, LaSarre B, Harwood CS, McKinlay JB. A purine salvage bottleneck leads to bacterial adenine cross-feeding. BioRxiv. 2023 Oct 10/17/2023; PMID: 37904951, PMCID: PMC10614841, PII: 2023.10.17.562681, DOI: 10.1101/2023.10.17.562681.
Worthan SB, McCarthy RDP, Behringer MG. Case Studies in the Assessment of Microbial Fitness: Seemingly Subtle Changes Can Have Major Effects on Phenotypic Outcomes. J Mol Evol [print-electronic]. 2023 Jun; 91(3): 311-24. PMID: 36752825, PMCID: PMC10276084, PII: 10.1007/s00239-022-10087-9, DOI: 10.1007/s00239-022-10087-9, ISSN: 1432-1432.
Zhao C, Kelly K, Jabbur ML, Paguaga M, Behringer M, Johnson CH. Host circadian behaviors exert only weak selective pressure on the gut microbiome under stable conditions but are critical for recovery from antibiotic treatment. PLoS Biol. 2022 Nov; 20(11): e3001865. PMID: 36350921, PMCID: PMC9645659, PII: PBIOLOGY-D-22-00791, DOI: 10.1371/journal.pbio.3001865, ISSN: 1545-7885.
Wei W, Ho WC, Behringer MG, Miller SF, Bcharah G, Lynch M. Rapid evolution of mutation rate and spectrum in response to environmental and population-genetic challenges. Nat Commun. 2022 Aug 8/13/2022; 13(1): 4752. PMID: 35963846, PMCID: PMC9376063, PII: 10.1038/s41467-022-32353-6, DOI: 10.1038/s41467-022-32353-6, ISSN: 2041-1723.
Behringer MG, Ho WC, Meraz JC, Miller SF, Boyer GF, Stone CJ, Andersen M, Lynch M. Complex Ecotype Dynamics Evolve in Response to Fluctuating Resources. MBio [print-electronic]. 2022 Jun 6/28/2022; 13(3): e0346721. PMID: 35575545, PMCID: PMC9239185, DOI: 10.1128/mbio.03467-21, ISSN: 2150-7511.
Ho WC, Behringer MG, Miller SF, Gonzales J, Nguyen A, Allahwerdy M, Boyer GF, Lynch M. Evolutionary Dynamics of Asexual Hypermutators Adapting to a Novel Environment. Genome Biol Evol. 2021 Dec 12/1/2021; 13(12): PMID: 34864972, PMCID: PMC8643662, PII: 6432043, DOI: 10.1093/gbe/evab257, ISSN: 1759-6653.
Behringer MG. Multi-omic Characterization of Intraspecies Variation in Laboratory and Natural Environments. MSystems [print-electronic]. 2021 Aug 8/31/2021; 6(4): e0076421. PMID: 34427516, PMCID: PMC8409731, DOI: 10.1128/mSystems.00764-21, ISSN: 2379-5077.
Shoemaker WR, Jones SE, Muscarella ME, Behringer MG, Lehmkuhl BK, Lennon JT. Microbial population dynamics and evolutionary outcomes under extreme energy limitation. Proc Natl Acad Sci U S A. 2021 Aug 8/17/2021; 118(33): PMID: 34385301, PMCID: PMC8379937, PII: 2101691118, DOI: 10.1073/pnas.2101691118, ISSN: 1091-6490.
Fritts RK, Bird JT, Behringer MG, Lipzen A, Martin J, Lynch M, McKinlay JB. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J [print-electronic]. 2020 Nov; 14(11): 2816-28. PMID: 32788711, PMCID: PMC7784955, PII: 10.1038/s41396-020-00737-5, DOI: 10.1038/s41396-020-00737-5, ISSN: 1751-7370.
Kucukyildirim S, Behringer M, Sung W, Brock DA, Doak TG, Mergen H, Queller DC, Strassmann JE, Lynch M. Low Base-Substitution Mutation Rate but High Rate of Slippage Mutations in the Sequence Repeat-Rich Genome of Dictyostelium discoideum. G3 (Bethesda). 2020 Sep 9/2/2020; 10(9): 3445-52. PMID: 32732307, PMCID: PMC7466956, PII: g3.120.401578, DOI: 10.1534/g3.120.401578, ISSN: 2160-1836.
Kucukyildirim S, Behringer M, Williams EM, Doak TG, Lynch M. Estimation of the Genome-Wide Mutation Rate and Spectrum in the Archaeal Species Haloferax volcanii. Genetics [print-electronic]. 2020 Aug; 215(4): 1107-16. PMID: 32513815, PMCID: PMC7404244, PII: genetics.120.303299, DOI: 10.1534/genetics.120.303299, ISSN: 1943-2631.
Fallon TR, Lower SE, Chang CH, Bessho-Uehara M, Martin GJ, Bewick AJ, Behringer M, Debat HJ, Wong I, Day JC, Suvorov A, Silva CJ, Stanger-Hall KF, Hall DW, Schmitz RJ, Nelson DR, Lewis SM, Shigenobu S, Bybee SM, Larracuente AM, Oba Y, Weng JK. Firefly genomes illuminate parallel origins of bioluminescence in beetles. Elife. 2018 Oct 10/16/2018; 7: PMID: 30324905, PMCID: PMC6191289, PII: 36495, DOI: 10.7554/eLife.36495, ISSN: 2050-084X.
McCully AL, Behringer MG, Gliessman JR, Pilipenko EV, Mazny JL, Lynch M, Drummond DA, McKinlay JB. An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris. Appl Environ Microbiol [electronic-print]. 2018 Jul 7/15/2018; 84(14): PMID: 29728387, PMCID: PMC6029099, PII: AEM.00404-18, DOI: 10.1128/AEM.00404-18, ISSN: 1098-5336.
Behringer MG, Boothe DM, Thungrat K. Evaluation of a fluorescence resonance energy transfer quantitative polymerase chain reaction assay for identification of gyrA mutations conferring enrofloxacin resistance in canine urinary Escherichia coli isolates and canine urine specimens. Am J Vet Res. 2018 Jul; 79(7): 755-61. PMID: 29943633, DOI: 10.2460/ajvr.79.7.755, ISSN: 1943-5681.
Behringer MG, Choi BI, Miller SF, Doak TG, Karty JA, Guo W, Lynch M. Escherichia coli cultures maintain stable subpopulation structure during long-term evolution. Proc Natl Acad Sci U S A [print-electronic]. 2018 May 5/15/2018; 115(20): E4642-E4650. PMID: 29712844, PMCID: PMC5960275, PII: 1708371115, DOI: 10.1073/pnas.1708371115, ISSN: 1091-6490.
Tincher C, Long H, Behringer M, Walker N, Lynch M. The Glyphosate-Based Herbicide Roundup Does not Elevate Genome-Wide Mutagenesis of Escherichia coli. G3 (Bethesda). 2017 Oct 10/5/2017; 7(10): 3331-5. PMID: 28983068, PMCID: PMC5633383, PII: g3.117.300133, DOI: 10.1534/g3.117.300133, ISSN: 2160-1836.
Long H, Behringer MG, Williams E, Te R, Lynch M. Similar Mutation Rates but Highly Diverse Mutation Spectra in Ascomycete and Basidiomycete Yeasts. Genome Biol Evol. 2016 Dec 12/1/2016; 8(12): 3815-21. PMID: 28173099, PMCID: PMC5521736, PII: 2737491, DOI: 10.1093/gbe/evw286, ISSN: 1759-6653.
Behringer MG, Hall DW. Selection on Position of Nonsense Codons in Introns. Genetics [print-electronic]. 2016 Nov; 204(3): 1239-48. PMID: 27630196, PMCID: PMC5105854, PII: genetics.116.189894, DOI: 10.1534/genetics.116.189894, ISSN: 1943-2631.
Behringer MG, Hall DW. The repeatability of genome-wide mutation rate and spectrum estimates. Curr Genet [print-electronic]. 2016 Aug; 62(3): 507-12. PMID: 26919990, PMCID: PMC4930417, PII: 10.1007/s00294-016-0573-7, DOI: 10.1007/s00294-016-0573-7, ISSN: 1432-0983.
Behringer MG, Hall DW. Genome-Wide Estimates of Mutation Rates and Spectrum in Schizosaccharomyces pombe Indicate CpG Sites are Highly Mutagenic Despite the Absence of DNA Methylation. G3 (Bethesda). 2015 Nov 11/12/2015; 6(1): 149-60. PMID: 26564949, PMCID: PMC4704713, PII: g3.115.022129, DOI: 10.1534/g3.115.022129, ISSN: 2160-1836.
Behringer M, Miller WG, Oyarzabal OA. Typing of Campylobacter jejuni and Campylobacter coli isolated from live broilers and retail broiler meat by flaA-RFLP, MLST, PFGE and REP-PCR. J Microbiol Methods [print-electronic]. 2011 Feb; 84(2): 194-201. PMID: 21130125, PII: S0167-7012(10)00395-7, DOI: 10.1016/j.mimet.2010.11.016, ISSN: 1872-8359.
Miller RS, Miller WG, Behringer M, Hariharan H, Matthew V, Oyarzabal OA. DNA identification and characterization of Campylobacter jejuni and Campylobacter coli isolated from caecal samples of chickens in Grenada. J Appl Microbiol [print-electronic]. 2010 Mar; 108(3): 1041-9. PMID: 19735321, DOI: 10.1111/j.1365-2672.2009.04507.x, ISSN: 1365-2672.
Worthan SB, McCarthy RDP, Delaleau M, Stikeleather R, Bratton BP, Boudvillain M, Behringer MG. Evolution of pH-sensitive transcription termination during adaptation to repeated long-term starvation. BioRxiv. 2024 Mar 3/1/2024; PMID: 38464051, PMCID: PMC10925284, PII: 2024.03.01.582989, DOI: 10.1101/2024.03.01.582989.
Chuang YC, Haas NW, Pepin R, Behringer MG, Oda Y, LaSarre B, Harwood CS, McKinlay JB. Bacterial adenine cross-feeding stems from a purine salvage bottleneck. ISME J. 2024 Jan 1/8/2024; 18(1): PMID: 38452196, PMCID: PMC10976475, PII: 7624067, DOI: 10.1093/ismejo/wrae034, ISSN: 1751-7370.
Stone CJ, Boyer GF, Behringer MG. Differential adenine methylation analysis reveals increased variability in 6mA in the absence of methyl-directed mismatch repair. MBio [print-electronic]. 2023 Oct 10/31/2023; 14(5): e0128923. PMID: 37796009, PMCID: PMC10653831, DOI: 10.1128/mbio.01289-23, ISSN: 2150-7511.
Chuang YC, Haas NW, Pepin R, Behringer M, Oda Y, LaSarre B, Harwood CS, McKinlay JB. A purine salvage bottleneck leads to bacterial adenine cross-feeding. BioRxiv. 2023 Oct 10/17/2023; PMID: 37904951, PMCID: PMC10614841, PII: 2023.10.17.562681, DOI: 10.1101/2023.10.17.562681.
Worthan SB, McCarthy RDP, Behringer MG. Case Studies in the Assessment of Microbial Fitness: Seemingly Subtle Changes Can Have Major Effects on Phenotypic Outcomes. J Mol Evol [print-electronic]. 2023 Jun; 91(3): 311-24. PMID: 36752825, PMCID: PMC10276084, PII: 10.1007/s00239-022-10087-9, DOI: 10.1007/s00239-022-10087-9, ISSN: 1432-1432.
Zhao C, Kelly K, Jabbur ML, Paguaga M, Behringer M, Johnson CH. Host circadian behaviors exert only weak selective pressure on the gut microbiome under stable conditions but are critical for recovery from antibiotic treatment. PLoS Biol. 2022 Nov; 20(11): e3001865. PMID: 36350921, PMCID: PMC9645659, PII: PBIOLOGY-D-22-00791, DOI: 10.1371/journal.pbio.3001865, ISSN: 1545-7885.
Wei W, Ho WC, Behringer MG, Miller SF, Bcharah G, Lynch M. Rapid evolution of mutation rate and spectrum in response to environmental and population-genetic challenges. Nat Commun. 2022 Aug 8/13/2022; 13(1): 4752. PMID: 35963846, PMCID: PMC9376063, PII: 10.1038/s41467-022-32353-6, DOI: 10.1038/s41467-022-32353-6, ISSN: 2041-1723.
Behringer MG, Ho WC, Meraz JC, Miller SF, Boyer GF, Stone CJ, Andersen M, Lynch M. Complex Ecotype Dynamics Evolve in Response to Fluctuating Resources. MBio [print-electronic]. 2022 Jun 6/28/2022; 13(3): e0346721. PMID: 35575545, PMCID: PMC9239185, DOI: 10.1128/mbio.03467-21, ISSN: 2150-7511.
Ho WC, Behringer MG, Miller SF, Gonzales J, Nguyen A, Allahwerdy M, Boyer GF, Lynch M. Evolutionary Dynamics of Asexual Hypermutators Adapting to a Novel Environment. Genome Biol Evol. 2021 Dec 12/1/2021; 13(12): PMID: 34864972, PMCID: PMC8643662, PII: 6432043, DOI: 10.1093/gbe/evab257, ISSN: 1759-6653.
Behringer MG. Multi-omic Characterization of Intraspecies Variation in Laboratory and Natural Environments. MSystems [print-electronic]. 2021 Aug 8/31/2021; 6(4): e0076421. PMID: 34427516, PMCID: PMC8409731, DOI: 10.1128/mSystems.00764-21, ISSN: 2379-5077.
Shoemaker WR, Jones SE, Muscarella ME, Behringer MG, Lehmkuhl BK, Lennon JT. Microbial population dynamics and evolutionary outcomes under extreme energy limitation. Proc Natl Acad Sci U S A. 2021 Aug 8/17/2021; 118(33): PMID: 34385301, PMCID: PMC8379937, PII: 2101691118, DOI: 10.1073/pnas.2101691118, ISSN: 1091-6490.
Fritts RK, Bird JT, Behringer MG, Lipzen A, Martin J, Lynch M, McKinlay JB. Enhanced nutrient uptake is sufficient to drive emergent cross-feeding between bacteria in a synthetic community. ISME J [print-electronic]. 2020 Nov; 14(11): 2816-28. PMID: 32788711, PMCID: PMC7784955, PII: 10.1038/s41396-020-00737-5, DOI: 10.1038/s41396-020-00737-5, ISSN: 1751-7370.
Kucukyildirim S, Behringer M, Sung W, Brock DA, Doak TG, Mergen H, Queller DC, Strassmann JE, Lynch M. Low Base-Substitution Mutation Rate but High Rate of Slippage Mutations in the Sequence Repeat-Rich Genome of Dictyostelium discoideum. G3 (Bethesda). 2020 Sep 9/2/2020; 10(9): 3445-52. PMID: 32732307, PMCID: PMC7466956, PII: g3.120.401578, DOI: 10.1534/g3.120.401578, ISSN: 2160-1836.
Kucukyildirim S, Behringer M, Williams EM, Doak TG, Lynch M. Estimation of the Genome-Wide Mutation Rate and Spectrum in the Archaeal Species Haloferax volcanii. Genetics [print-electronic]. 2020 Aug; 215(4): 1107-16. PMID: 32513815, PMCID: PMC7404244, PII: genetics.120.303299, DOI: 10.1534/genetics.120.303299, ISSN: 1943-2631.
Fallon TR, Lower SE, Chang CH, Bessho-Uehara M, Martin GJ, Bewick AJ, Behringer M, Debat HJ, Wong I, Day JC, Suvorov A, Silva CJ, Stanger-Hall KF, Hall DW, Schmitz RJ, Nelson DR, Lewis SM, Shigenobu S, Bybee SM, Larracuente AM, Oba Y, Weng JK. Firefly genomes illuminate parallel origins of bioluminescence in beetles. Elife. 2018 Oct 10/16/2018; 7: PMID: 30324905, PMCID: PMC6191289, PII: 36495, DOI: 10.7554/eLife.36495, ISSN: 2050-084X.
McCully AL, Behringer MG, Gliessman JR, Pilipenko EV, Mazny JL, Lynch M, Drummond DA, McKinlay JB. An Escherichia coli Nitrogen Starvation Response Is Important for Mutualistic Coexistence with Rhodopseudomonas palustris. Appl Environ Microbiol [electronic-print]. 2018 Jul 7/15/2018; 84(14): PMID: 29728387, PMCID: PMC6029099, PII: AEM.00404-18, DOI: 10.1128/AEM.00404-18, ISSN: 1098-5336.
Behringer MG, Boothe DM, Thungrat K. Evaluation of a fluorescence resonance energy transfer quantitative polymerase chain reaction assay for identification of gyrA mutations conferring enrofloxacin resistance in canine urinary Escherichia coli isolates and canine urine specimens. Am J Vet Res. 2018 Jul; 79(7): 755-61. PMID: 29943633, DOI: 10.2460/ajvr.79.7.755, ISSN: 1943-5681.
Behringer MG, Choi BI, Miller SF, Doak TG, Karty JA, Guo W, Lynch M. Escherichia coli cultures maintain stable subpopulation structure during long-term evolution. Proc Natl Acad Sci U S A [print-electronic]. 2018 May 5/15/2018; 115(20): E4642-E4650. PMID: 29712844, PMCID: PMC5960275, PII: 1708371115, DOI: 10.1073/pnas.1708371115, ISSN: 1091-6490.
Tincher C, Long H, Behringer M, Walker N, Lynch M. The Glyphosate-Based Herbicide Roundup Does not Elevate Genome-Wide Mutagenesis of Escherichia coli. G3 (Bethesda). 2017 Oct 10/5/2017; 7(10): 3331-5. PMID: 28983068, PMCID: PMC5633383, PII: g3.117.300133, DOI: 10.1534/g3.117.300133, ISSN: 2160-1836.
Long H, Behringer MG, Williams E, Te R, Lynch M. Similar Mutation Rates but Highly Diverse Mutation Spectra in Ascomycete and Basidiomycete Yeasts. Genome Biol Evol. 2016 Dec 12/1/2016; 8(12): 3815-21. PMID: 28173099, PMCID: PMC5521736, PII: 2737491, DOI: 10.1093/gbe/evw286, ISSN: 1759-6653.
Behringer MG, Hall DW. Selection on Position of Nonsense Codons in Introns. Genetics [print-electronic]. 2016 Nov; 204(3): 1239-48. PMID: 27630196, PMCID: PMC5105854, PII: genetics.116.189894, DOI: 10.1534/genetics.116.189894, ISSN: 1943-2631.
Behringer MG, Hall DW. The repeatability of genome-wide mutation rate and spectrum estimates. Curr Genet [print-electronic]. 2016 Aug; 62(3): 507-12. PMID: 26919990, PMCID: PMC4930417, PII: 10.1007/s00294-016-0573-7, DOI: 10.1007/s00294-016-0573-7, ISSN: 1432-0983.
Behringer MG, Hall DW. Genome-Wide Estimates of Mutation Rates and Spectrum in Schizosaccharomyces pombe Indicate CpG Sites are Highly Mutagenic Despite the Absence of DNA Methylation. G3 (Bethesda). 2015 Nov 11/12/2015; 6(1): 149-60. PMID: 26564949, PMCID: PMC4704713, PII: g3.115.022129, DOI: 10.1534/g3.115.022129, ISSN: 2160-1836.
Behringer M, Miller WG, Oyarzabal OA. Typing of Campylobacter jejuni and Campylobacter coli isolated from live broilers and retail broiler meat by flaA-RFLP, MLST, PFGE and REP-PCR. J Microbiol Methods [print-electronic]. 2011 Feb; 84(2): 194-201. PMID: 21130125, PII: S0167-7012(10)00395-7, DOI: 10.1016/j.mimet.2010.11.016, ISSN: 1872-8359.
Miller RS, Miller WG, Behringer M, Hariharan H, Matthew V, Oyarzabal OA. DNA identification and characterization of Campylobacter jejuni and Campylobacter coli isolated from caecal samples of chickens in Grenada. J Appl Microbiol [print-electronic]. 2010 Mar; 108(3): 1041-9. PMID: 19735321, DOI: 10.1111/j.1365-2672.2009.04507.x, ISSN: 1365-2672.