Research

Community characterization and functional analysis of microbiomes of farm animals

The microbiome of mammals contributes significantly to various fundamental aspects of function and health. Whereas the human microbiome has been studied in great detail and depth, the microbiomes of farm animals are much less well known. Our research focuses on analyzing the variation in the microbiomes in farm animals in response to different nutrition and disease conditions. One main focus of our research are bacteria attached to the rumen wall (also called “epimural” bacteria), as the rumen wall is the central interface between the host and its ruminal microbiota. Most of the current research on microbiota describes communities at different times and conditions (i.e. “who is there”). While this is an important first step, we are applying functional analyses by using metagenome shotgun and metatranscriptome sequencing as tools to analyze the functional capacity (“what can they do”) function and activity of microbiota in situ (“what are they doing”). Both descriptive and functional methods are thus essential for our research. One of our main aims is to understand the interactions between bacteria and farm animals focusing on basic research questions, such as e.g. nutrition and disease. Interdisciplinary research is essential in order to understand the complex interaction between animals and their microbiota, and to improve animal production without compromising animal health.

Selected Publications:

  • Wetzels SU, Mann E, Pourazad P, Qumar M, Pinior B, Metzler-Zebeli BU, Wagner M, Schmitz-Esser S, Zebeli Q. 2017. Epimural bacterial community structure in the rumen of Holstein cows with different responses to a long-term subacute ruminal acidosis diet challenge. J. Dairy Sci. 100:1829–1844
  • Wetzels SU, Mann E, Metzler-Zebeli BU, Pourazad P, Qumar M, Klevenhusen F, Pinior B, Wagner M, Zebeli Q, Schmitz-Esser S. 2016. Epimural indicator phylotypes of transiently-induced subacute ruminal acidosis in dairy cattle. Front. Microbiol. 7:274
  • Mann E, Wetzels SU, Pinior B, Metzler-Zebeli BU, Wagner M, Schmitz-Esser S. 2016. Psychrophile spoilers dominate the bacterial microbiome in musculature samples of slaughter pigs. Meat Sci. 117:36-40.
  • Mann E, Pinior B, Wetzels SU, Metzler-Zebeli BU, Wagner M, Schmitz-Esser S. 2015. The metabolically active bacterial microbiome of tonsils and mandibular lymph nodes of slaughter pigs. Front. Microbiol. 6:1362. doi: 10.3389/fmicb.2015.01362
  • Mann E, Dzieciol M, Pinior B, Neubauer V, Metzler-Zebeli BU, Wagner M, Schmitz-Esser S. High diversity of viable bacteria isolated from lymph nodes of slaughter pigs and its possible impacts for food safety. 2015. J Appl Microbiol. 119(5):1420-1432
  • Wetzels S. U., Mann E, Metzler-Zebeli B. U., Wagner M., Klevenhusen F., Zebeli Q., Schmitz-Esser S. Pyrosequencing reveals shifts in the bacterial epimural community relative to dietary concentrate amount in goats. 2015. J. Dairy Sci. 98(8):5572-87.
  • Klein-Jöbstl D, Schornsteiner E, Mann E, Wagner M, Drillich M, Schmitz-Esser S. 2014. Pyrosequencing reveals diverse fecal microbiota in Simmental calves during early development. Front. Microbiol. 17;5:622.
  • Mann E., Dzieciol M., Metzler-Zebeli B. U., Wagner M., Schmitz-Esser S. 2014. Microbiomes of unreactive and pathologically altered ileocecal lymph nodes of slaughter pigs. Appl. Environ. Microbiol. 80:193-203.

 

Food safety – persistence of Listeria monocytogenes in food production environments

The food-borne pathogen Listeria monocytogenes is a great concern for food safety because of the high mortality rate associated with listeriosis and also because of the wide occurrence of Listeria monocytogenes in food production environments. Furthermore, the long-term survival of Listeria monocytogenes in food production plants – which is also called “persistence”, poses additional risks on food safety. However, the molecular mechanisms enabling the persistence of Listeria monocytogenes are still largely unknown. To elucidate molecular mechanisms of Listeria monocytogenes persistence, we apply community characterization and whole genome sequencing as hypothesis-generating tools and post-genomic analyses, such as functional characterization of deletion mutants to identify genetic determinants possibly involved in persistence, to verify hypotheses generated during genome sequencing. In order to improve food safety, a detailed knowledge on the molecular mechanisms underlying survival of Listeria monocytogenes is needed.

Selected publications:

  • Rychli K, Wagner EM, Ciolacu L, Zaiser A, Tasara T, Wagner M, Schmitz-Esser S. 2017. Comparative genomics of human and non-human Listeria monocytogenes sequence type 121 strains. PLoS One. 12(5):e0176857.
  • Schön K, Schornsteiner E, Dzieciol M, Wagner M, Müller M, Schmitz-Esser S. 2016. Microbial communities in dairy processing environment floor-drains are dominated by product-associated bacteria and yeasts. Food Control. 70, 210-215.
  • Dzieciol M, Schornsteiner E, Muhterem-Uyar M, Stessl B, Wagner M, Schmitz-Esser S. 2016. Bacterial diversity of floor drain biofilms and drain waters in a Listeria monocytogenes contaminated food processing environment. Int J Food Microbiol. 223:33-40.
  • Schmitz-Esser S., Müller A., Wagner M. Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages. 2015. Front. Microbiol. 28;6:380.
  • Müller A, Rychli K, Zaiser A, Wieser C, Wagner M, Schmitz-Esser S. 2014. The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol. Lett. 361(2):166-73.
  • Rychli K., Müller A., Zaiser A., Schoder D., Allerberger F., Wagner M., Schmitz-Esser S. 2014. Genome sequencing of Listeria monocytogenes "Quargel" listeriosis outbreak strains reveals two different strains with distinct in vitro virulence potential. PLoS One. 9:e89964.
  • Müller A., Rychli K., Muhterem-Uyar M., Zaiser A., Stessl B., Guinane C. M., Cotter P. D., Wagner M., Schmitz-Esser S. 2013. Tn6188 - a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS One. 8:e76835.

 

Symbiosis research - Host cell interaction of the insect symbiont Cardinium hertigii

In the course of my PhD studies and my first postdoc years, I worked with obligate intracellular bacterial symbionts of amoebae and investigated how these symbionts interact with their host cells. One focus was the characterization of nucleotide transport proteins which are used by the symbionts to import nucleotides from the host, to compensate for their inability to synthesize nucleotides themselves. Our analysis of the genome sequence of the obligate intracellular amoeba symbiont Amoebophilus asiaticus, a member of the Bacteroidetes, revealed that this bacterium coded for an extraordinarily high abundance of proteins harboring eukaryotic domains and transposases. We also identified what we speculate is an entirely novel prophage-related secretion system and performed whole transcriptome sequencing of Amoebophilus asiaticus and its amoeba host.

In collaboration with Prof. Molly Hunter in the Department of Entomology from the University of Arizona we are working on the insect symbiont Cardinium hertigii – the sister clade of Amoebophilus asiaticus - which is special due to its ability to manipulate the reproduction of its insect host - a fundamental alteration of early embryogenesis that has been called cytoplasmic incompatibility, only the second bacterial lineage known to be capable of this manipulation. This research resulted in a publication showing that cytoplasmic incompatibility evolved independently in Cardinium. We are currently applying genome sequencing and metatranscriptome sequencing to analyze the molecular mechanisms for host cell manipulation of this elusive symbiont and its host in more detail.

Selected Publications:

  • Haferkamp I, Penz T, Geier M, Ast M, Mushak T, Horn M, Schmitz-Esser S. The endosymbiont Amoebophilus asiaticus encodes an S-adenosylmethionine carrier that compensates for its missing methylation cycle. 2013. J Bacteriol. 195(14):3183-92.
  • Penz T., Schmitz-Esser S, Kelly S.E., Cass B.N., Müller A., Woyke T., Malfatti S.A., Hunter M.S., Horn M. 2012. Comparative genomics suggests an independent origin of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genet., 8(10):e1003012.
  • Schmitz-Esser S, T. Penz, A. Spang, M. Horn. 2011. A bacterial genome in transition - an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus. BMC Evol. Biol., 11:270.
  • Penz T, M. Horn, S. Schmitz-Esser. 2010. The genome of the amoeba symbiont "Candidatus Amoebophilus asiaticus" encodes an afp-like prophage possibly used for protein secretion. Virulence, 1(6):541-5.
  • Schmitz-Esser S., P. Tischler, R. Arnold, J. Montanaro, M. Wagner, T. Rattei, and M. Horn. 2010. The genome of the amoeba symbiont ‘Candidatus Amoebophilus asiaticus’ reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J. Bacteriol., 192(4):1045-57.
  • Schmitz-Esser S., E.R. Toenshoff, S. Haider, E. Heinz, V.M. Hoenninger, M. Wagner, and M. Horn. 2008. Diversity of bacterial endosymbionts of environmental Acanthamoeba isolates. Appl. Environ. Microbiol., 74:5822-5831.
  • Haferkamp I., S. Schmitz-Esser, M. Wagner, N. Neigel, M. Horn, and H. E. Neuhaus. 2006. Tapping the nucleotide pool of the host: novel nucleotide carrier proteins of Protochlamydia amoebophila. Mol. Microbiol., 60: 1534-1545.
  • Haferkamp I., S. Schmitz-Esser, N. Linka, C. Urbany, A. Collingro, M. Wagner, M. Horn, H. E. Neuhaus. 2004. A candidate NAD+ transporter in an intracellular bacterial symbiont related to chlamydiae. Nature, 432: 622-625.
  • Schmitz-Esser S., N. Linka, A. Collingro, C. L. Beier, H. E. Neuhaus, M. Wagner, M. Horn. 2004. ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to chlamydiae and rickettsiae. J. Bacteriol., 186:683-691.