One focus of our research are obligate intracellular bacterial symbionts of amoebae and we 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 Dr. Molly Hunter in the Department of Entomology from the University of Arizona and Dr. Manuel Kleiner from North Carolina State University 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 have applied genome and transcriptome sequencing to analyze the molecular mechanisms for host cell manipulation of this elusive symbiont and its host in more detail.
Selected Publications:
- Schultz DL, Selberherr M, Stouthamer CM, Doremus MR, Kelly SE, Hunter MS, Schmitz-Esser S. 2022. Sex-based de novo transcriptome assemblies of the parasitoid wasp Encarsia suzannae, a host of the manipulative heritable symbiont Cardinium hertigii. Gigabyte. 10.46471/gigabyte.68
- Doremus MR, Stouthamer CM, Kelly SE, Schmitz-Esser S, Hunter MS. 2022. Quality over quantity: unraveling the contributions to cytoplasmic incompatibility caused by two coinfecting Cardinium symbionts. Heredity (Edinb). 128(3):187-195. doi: 10.1038/s41437-022-00507-3
- Selberherr E, Penz T, König L, Conrady B, Siegl A, Horn M, Schmitz-Esser S. 2022. The life cycle-dependent transcriptional profile of the obligate intracellular amoeba symbiont Amoebophilus asiaticus. FEMS Microbiol Ecol. 98(1):fiac001. doi: 10.1093/femsec/fiac001
- Doremus MR, Stouthamer CM, Kelly SE, Schmitz-Esser S, Hunter MS. 2020. Cardinium Localization During Its Parasitoid Wasp Host's Development Provides Insights Into Cytoplasmic Incompatibility. Front Microbiol; 11:606399. doi: 10.3389/fmicb.2020.606399.
- Stouthamer CM, Kelly SE, Mann E, Schmitz-Esser S, Hunter MS. 2019. Development of a Multi-Locus Sequence Typing System Helps Reveal the Evolution of Cardinium Hertigii, a Reproductive Manipulator Symbiont of Insects. BMC Microbiol. 19, 266
- Mann E, Stouthamer CM, Kelly SE, Dzieciol M, Hunter MS, Schmitz-Esser S. 2017. Transcriptome Sequencing Reveals Novel Candidate Genes for Cardinium hertigii-Caused Cytoplasmic Incompatibility and Host-Cell Interaction. mSystems. 2(6). pii: e00141-17
- 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.
Funding Organization: National Science Foundation
Award Number: 2002987