SFB 987:  Microbial Diversity in Environmental Signal Response

• Subject Area: Biology ; Medicine
• Term: from 2012 to 2020
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 192445154

• Final Report Year: 2020

Final Report Abstract

Microorganisms provide the greatest diversity if life on earth. They successfully colonize every conceivable ecological niche, regardless of its welcoming or hostile conditions. Microorganisms do so either as highly specialized individual cells or as complex structured microbial communities. For most bacteria and fungi there is only one certainty: Change! The aim of the CRC 987 was to extend our knowledge on the mechanistic diversity allowing microorganisms to perceive, process and respond to intra- and extracellular cues to meet arising challenges. During its 2 nd funding period, the PIs working in research area D of the CRC 987 made several seminal contributions allowing an understanding of the metabolic adaptions of microorganisms in response to environmental changes. These range from the in-depth clarification of condition-specific metabolic pathways and their adjustment in response to cellular and environmental disturbances. Complementary, the PIs of research area E provided in-depth insights into how prokaryotic and eukaryotic microorganisms adapt to environ- mental changes by adjusting cellular surface structures such as polysaccharides, flagella and various types of cell appendices. In summary, during the second funding period, the members of both research areas of the CRC 987 con- tributed 127 publications, with 25 of them being jointly authored by at least two PIs; all manuscripts were published in internationally visible and peer-reviewed scientific journal. In addition, the PIs contributed re- view articles to a special issue of Biological Chemistry specifically dedicated to the overall research themes of the CRC 987 during its two funding periods. The CRC 987 has been a hub of scientific exchange, which is best exemplified by its seminar series (71 seminars during the two funding periods) in which 114 national and internationally renowned speakers reported cutting-edge findings in the field of Microbiology. In addition, the CRC 987 organized three inter- national conferences, and three theme-oriented workshops. Furthermore, the PIs of the CRC 987 served collectively as the principal organizers of the annual meeting of the German Society for General and Applied Microbiology (VAAM) in 2015 for which approximately 1.200 participants came to Marburg. From an educational point of view, 80 PhD theses linked to the overall research themes of the CRC 987, with an absolutely balanced gender ratio (50:50), were successfully completed. The advanced training of our doctoral students was enabled through the Marburg School of Microbiology and included a wide range of activities such as mandatory attendance to the CRC seminar series, thesis advisory measures, practical courses and on-site industry visits. To specifically prepare our female graduate students for their careers in either academia, industry, or government, seven workshops - conducted by an external company - were offered. These workshops were very well-received. Moreover, true highlights were the four “Spotlight Meet- ings in Microbiology” exclusively organized by our students together with those of the partnering CRC 766 from the University Tübingen. Despite the excellent performance of the CRC 987, especially during its 2 nd funding period, the PIs regret- tably had to decide not to apply to the DFG for a third funding period. This decision was not taken light- heartedly and only after intensive consultations among the PIs and with the president of the Philipps-Uni- versität. The reasoning for this decision simply reflects that six central PIs of the CRC 987 would not be able to participate for a full funding period due to their forthcoming retirement, and two young PIs decided to follow calls for full professorships to other universities. Thus, eight of the current 17 PIs would have to be replaced – a task which currently cannot be fulfilled in a timely manner.

Publications

• 2016. A minimal threshold of c-di-GMP is essential for fruiting body formation and sporulation in Myxococcus xanthus. PLoS Genet 12: e1006080
  Skotnicka D, Smaldone GT, Petters T, Trampari E, Liang J, Kaever V, Malone JG, Singer M, Søgaard-Andersen L
  
• 2016. Cyclic di-GMP regulates multiple cellular functions in the symbiotic alphaproteobacterium Sinorhizobium meliloti. J Bacteriol 198:521–535
  Schäper S, Krol E, Skotnicka D, Kaever V, Hilker R, Søgaard-Andersen L, Becker A
  
• 2016. Structural basis for the CsrA-dependent modulation of translation initiation by an ancient regulatory protein. Proc Natl Acad Sci U S A 113:10168–10173
  Altegoer F, Rensing SA, Bange G
  
• 2016. White collar 1-induced photolyase expression contributes to UV-tolerance of Ustilago maydis. Microbiologyopen 5:224–243
  Brych A, Mascarenhas J, Jaeger E, Charkiewicz E, Pokorny R, Bölker M, Doehlemann G, Batschauer A
  
• 2017. AraC-like transcriptional activator CuxR binds c-di-GMP by a PilZ-like mechanism to regulate extracellular polysaccharide production. Proc Natl Acad Sci U S A 114:E4822-E4831
  Schäper S, Steinchen W, Krol E, Altegoer F, Skotnicka D, Søgaard-Andersen L, Bange G, Becker A
  
• 2017. Evolutionary conservation and in vitro reconstitution of microsporidian iron-sulfur cluster biosynthesis. Nat Commun 8:13932
  Freibert S-A, Goldberg AV, Hacker C, Molik S, Dean P, Williams TA, Nakjang S, Long S, Sendra K, Bill E, Heinz E, Hirt RP, Lucocq JM, Embley TM, Lill R
  
• 2017. Hyperactivity of the Arabidopsis cryptochrome (cry1) L407F mutant is caused by a structural alteration close to the cry1 ATP-binding site. J Biol Chem 292:12906–12920
  Orth C, Niemann N, Hennig L, Essen L-O, Batschauer A
  
• 2017. Response of Methylocystis sp. strain SC2 to salt stress: physiology, global transcriptome, and amino acid profiles. Appl Environ Microbiol 83:e00866-17
  Han D, Link H, Liesack W
  
• 2017. Response of Methylocystis sp. strain SC2 to salt stress: Physiology, global transcriptome, and amino acid profiles. Appl Environ Microbiol 83:e00866-17
  Han D, Link H, Liesack W
  
• 2017. Sinorhizobium meliloti YbeY is an endoribonuclease with unprecedented catalytic features, acting as silencing enzyme in riboregulation. Nucl Acids Res 45:1371-1391
  Saramago M, Peregrina A, Robledo M, Matos RG, Hilker R, Serrania J, Becker A, Arraiano CM, Jiménez-Zurdo JI
  
• 2018. Fiberassociated spirochetes are major agents of hemicellulose degradation in the hindgut of wood-feeding higher termites. Proc Natl Acad Sci U S A 115: E11996-E12004
  Tokuda G, Mikaelyan A, Fukui C, Matsuura Y, Watanabe H, Fujishima M, Brune A
  
• 2018. Optimizing CRISPR/Cas9 for the diatom Phaeodactylum tricornutum. Front Plant Sci 9:740
  Stukenberg D, Zauner S, Dell'Aquila G, Maier UG
  
• 2018. Replacing the ethylmalonyl-CoA pathway with the glyoxylate shunt provides metabolic flexibility in the central carbon metabolism of Methylobacterium extorquens AM1. ACS Synth Biol 7:86–97
  Schada von Borzyskowski L, Sonntag F, Pöschel L, Vorholt JA, Schrader J, Erb TJ, Buchhaupt M
  
• 2018. Selective enrichment of slow-growing bacteria in a metabolism-wide CRISPRi library with a TIMER protein. ACS Synth Biol 7:2775–2782
  Beuter D, Gomes-Filho JV, Randau L, Díaz-Pascual F, Drescher K, Link H
  
• 2018. Seven-transmembrane receptor protein RgsP and cell wall-binding protein RgsM promote unipolar growth in Rhizobiales. PLoS Genet 14:e1007594
  Schäper S, Yau HCL, Krol E, Skotnicka D, Heimerl T, Gray J, Kaever V, Søgaard-Andersen L, Vollmer W, Becker A
  
• 2018. Structural and functional characterization of PA14/Flo5-like adhesins from Komagataella pastoris. Front Microbiol 9:2581
  Kock M, Brückner S, Wozniak N, Maestre-Reyna M, Veelders M, Schlereth J, Mösch H-U, Essen L-O
  
• 2018. Structural and functional characterization of PA14/Flo5-like adhesins from Komagataella pastoris. Front Microbiol 9:2581
  Kock M, Brückner S, Wozniak N, Maestre-Reyna M, Veelders M, Schlereth J, Mösch HU, Essen LO
  
• 2018. The multicatalytic compartment of propionyl-CoA synthase sequesters a toxic metabolite. Nat Chem Biol 14:1127–1132
  Bernhardsgrütter I, Vögeli B, Wagner T, Peter DM, Cortina NS, Kahnt J, Bange G, Engilberge S, Girard E, Riobé F, Maury O, Shima S, Zarzycki J, Erb TJ
  
• 2019. A kiwellin disarms the metabolic activity of a secreted fungal virulence factor. Nature 565:650–653
  Han X, Altegoer F, Steinchen W, Binnebesel L, Schuhmacher J, Glatter T, Giammarinaro PI, Djamei A, Rensing SA, Reissmann S, Kahmann R, Bange G
  
• 2019. Biosynthesis of the Stress-Protectant and Chemical Chaperon Ectoine: Biochemistry of the transaminase EctB. Front Microbiol 10:2811
  Richter AA, Mais C-N, Czech L, Geyer K, Hoeppner A, Smits SHJ, Erb TJ, Bange G, Bremer E
  
• 2019. Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function. Nat Microbiol 4:2136–2145
  Díaz-Pascual F, Hartmann R, Lempp M, Vidakovic L, Song B, Jeckel H, Thormann KM, Yildiz FH, Dunkel J, Link H, Nadell CD, Drescher K
  
• 2019. Breakdown of Vibrio cholerae biofilm architecture induced by antibiotics disrupts community barrier function. Nat Microbiol 4:2136–2145
  Díaz-Pascual F, Hartmann R, Lempp M, Vidakovic L, Song B, Jeckel H, Thormann KM, Yildiz FH, Dunkel J, Link H, Nadell CD, Drescher K
  
• 2019. Dynamic metabolic rewiring enables efficient acetyl coenzyme A assimilation in Paracoccus denitrificans. mBio 10:e00805-19
  Kremer K, van Teeseling MCF, Schada von Borzyskowski L, Bernhardsgrütter I, van Spanning RJM, Gates AJ, Remus-Emsermann MNP, Thanbichler M, Erb TJ.
  
• 2019. Exploiting substrate promiscuity of ectoine hydroxylase for regio- and stereoselective modification of homoectoine. Front Microbiol 10:2745
  Czech L, Wilcken S, Czech O, Linne U, Brauner J, Smits SHJ, Galinski EA, Bremer E
  
• 2019. Illuminating the catalytic core of ectoine synthase through structural and biochemical analysis. Sci Rep 9:364
  Czech L, Höppner A, Kobus S, Seubert A, Riclea R, Dickschat JS, Heider J, Smits SHJ, Bremer E
  
• 2019. Marine Proteobacteria metabolize glycolate via the β-hydroxyaspartate cycle. Nature 575:500–504
  Schada von Borzyskowski L, Severi F, Krüger K, Hermann L, Gilardet A, Sippel F, Pommerenke B, Claus P, Cortina NS, Glatter T, Zauner S, Zarzycki J, Fuchs BM, Bremer E, Maier UG, Amann RI, Erb TJ
  
• 2019. Opsin 1 and opsin 2 of the corn smut fungus Ustilago maydis are green light-driven proton pumps. Front Microbiol 10:735
  Panzer S, Brych A, Batschauer A, Terpitz U
  
• 2019. Structure and interaction of the archaeal motility repression module ArnA-ArnB that regulates archaellum expression in Sulfolobus acidocaldarius. J. Biol. Chem. 294: 7460-7474
  Hoffmann L, Anders K, Bischof L, Ye X, Reimann J, Khadouma S, Pham T, van der Does C, Wright P, Essen LO, Albers SV
  
• 2019. Systematic identification of metabolites controlling gene expression in E. coli. Nat Commun 10:4463
  Lempp M, Farke N, Kuntz M, Freibert SA, Lill R, Link H
  
• 2020 Metabolism of non-growing bacteria. Biol Chem.
  Lempp M, Lubrano P, Gert B, Link H
  
• 2020. BacStalk: A comprehensive and interactive image analysis software tool for bacterial cell biology. Mol Microbiol 114:140–150
  Hartmann R, van Teeseling MCF, Thanbichler M, Drescher K
  
• 2020. CdbA is a DNA-binding protein and c-di-GMP receptor important for nucleoid organization and segregation in Myxococcus xanthus. Nat Commun 11:1791
  Skotnicka D, Steinchen W, Szadkowski D, Cadby IT, Lovering AL, Bange G, Søgaard-Andersen L
  
• 2020. Cyclic di-GMP signaling in Bacillus subtilis is governed by direct interactions of diguanylate cyclases and cognate receptors. mBio 11: e03122-19
  Kunz S, Tribensky A, Steinchen W, Oviedo-Bocanegra L, Bedrunka P, Graumann PL
  
• 2020. Degradation of the microbial stress protectants and chemical chaperones ectoine and hydroxyectoine by a bacterial hydrolase-deacetylase complex. J Biol Chem 295:9087–9104
  Mais C-N, Hermann L, Altegoer F, Seubert A, Richter AA, Wernersbach I, Czech L, Bremer E, Bange G
  
• 2020. Functional reprogramming of Candida glabrata epithelial adhesins: the role of conserved and variable structural motifs in ligand binding. J Biol Chem. 295:12512-12524
  Hoffmann D, Diderrich R, Reithofer V, Friederichs S, Kock M, Essen L-O, Mösch H-U
  
• 2020. Integrative and quantitative view of the CtrA regulatory network in a stalked budding bacterium. PLoS Genet 16: e1008724
  Leicht O, van Teeseling MCF, Panis G, Reif C, Wendt H, Viollier PH, Thanbichler M
  
• 2020. Kin discrimination in social yeast is mediated by cell surface receptors of the Flo11 adhesin family. Elife 9:e55587
  Brückner S, Schubert R, Kraushaar T, Hartmann R, Hoffmann D, Jelli E, Drescher K, Müller DJ, Essen O-L, Mösch H-U
  
• 2020. Peroxisomal targeting of a protein phosphatase type 2C via mitochondrial transit. Nat Commun 11:2355
  Stehlik T, Kremp M, Kahnt J, Bölker M, Freitag J
  
• 2020. Structural base for the transfer of GPI-anchored glycoproteins into fungal cell walls. Proc Natl Acad Sci U S A
  Vogt MS, Schmitz GF, Varón Silva D, Mösch H-U, Essen L-O
  
• 2020. The architecture of the diaminobutyrate acetyltransferase active site provides mechanistic insight into the biosynthesis of the chemical chaperone ectoine. J Biol Chem 295:2822–2838
  Richter AA, Kobus S, Czech L, Hoeppner A, Zarzycki J, Erb TJ, Lauterbach L, Dickschat JS, Bremer E, Smits SHJ