A cyclic lipopeptide produced by an antagonistic bacterium relies on its tail and transient receptor potential-type Ca
ADF1
Ca2+ channels
Chlamydomonas reinhardtii
Pseudomonas protegens
cilia/flagella
cyclic lipopeptides
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
received:
23
10
2022
accepted:
28
11
2022
pubmed:
6
12
2022
medline:
4
2
2023
entrez:
5
12
2022
Statut:
ppublish
Résumé
The antagonistic bacterium Pseudomonas protegens secretes the cyclic lipopeptide (CLiP) orfamide A, which triggers a Ca
Substances chimiques
Lipopeptides
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1620-1635Informations de copyright
© 2022 The Authors New Phytologist © 2022 New Phytologist Foundation.
Références
Aiyar P, Schaeme D, García-Altares M, Carrasco Flores D, Dathe H, Hertweck C, Sasso S, Mittag M. 2017. Antagonistic bacteria disrupt calcium homeostasis and immobilize algal cells. Nature Communications 8: 1-12.
Arias-Darraz L, Cabezas D, Colenso CK, Alegría-Arcos M, Bravo-Moraga F, Varas-Concha I, Almonacid DE, Madrid R, Brauchi S. 2015a. A transient receptor potential ion channel in Chlamydomonas shares key features with sensory transduction-associated TRP channels in mammals. Plant Cell 27: 177-188.
Arias-Darraz L, Colenso CK, Veliz LA, Vivar JP, Cardenas S, Brauchi S. 2015b. A TRP conductance modulates repolarization after sensory-dependent depolarization in Chlamydomonas reinhardtii. Plant Signaling and Behavior 10: e1052924.
Bando Y, Hou Y, Seyfarth L, Probst J, Götze S, Bogacz M, Hellmich UA, Stallforth P, Mittag M, Arndt H-D. 2022. Total synthesis and structure correction of the cyclic lipodepsipeptide orfamide A. Chemistry-A European Journal 28: e202104417.
Bickerton P, Sello S, Brownlee C, Pittman JK, Wheeler GL. 2016. Spatial and temporal specificity of Ca2+ signalling in Chlamydomonas reinhardtii in response to osmotic stress. New Phytologist 212: 920-933.
Cabezas-Bratesco D, Mcgee FA, Colenso CK, Zavala K, Granata D, Carnevale V, Opazo JC, Brauchi SE. 2022. Sequence and structural conservation reveal fingerprint residues in TRP channels. eLife 11: e73645.
Clapham DE. 2007. SnapShot: mammalian TRP channels. Cell 129: 220.
Colton CK, Zhu MX. 2007. 2-Aminoethoxydiphenyl borate as a common activator of TRPV1, TRPV2, and TRPV3 channels. Handbook of Experimental Pharmacology 179: 173-187.
Cooper MB, Smith AG. 2015. Exploring mutualistic interactions between microalgae and bacteria in the omics age. Current Opinion in Plant Biology 26: 147-153.
De Roo V, Verleysen Y, Kovács B, De Vleeschouwer M, Muangkaew P, Girard L, Höfte M, De Mot R, Madder A, Geudens N et al. 2022. An nuclear magnetic resonance fingerprint matching approach for the identification and structural re-evaluation of Pseudomonas lipopeptides. Microbiology Spectrum 10: e01261-22.
De Vleeschouwer M, Sinnaeve D, Van Den Begin J, Coenye T, Martins JC, Madder A. 2014. Rapid total synthesis of cyclic lipodepsipeptides as a premise to investigate their self-assembly and biological activity. Chemistry - A European Journal 20: 7766-7775.
De Vleeschouwer M, Van Kersavond T, Verleysen Y, Sinnaeve D, Coenye T, Martins JC, Madder A. 2020. Identification of the molecular determinants involved in antimicrobial activity of pseudodesmin A, a cyclic lipopeptide from the viscosin group. Frontiers in Microbiology 11: 646.
Delling M, Indzhykulian AA, Liu X, Li Y, Xie T, Corey DP, Clapham DE. 2016. Primary cilia are not calcium-responsive mechanosensors. Nature 531: 656-660.
Ferreira RR, Fukui H, Chow R, Vilfan A, Vermot J. 2019. The cilium as a force sensor−myth versus reality. Journal of Cell Science 132: jcs213496.
Fewer DP, Jokela J, Heinilä L, Aesoy R, Sivonen K, Galica T, Hrouzek P, Herfindal L. 2021. Chemical diversity and cellular effects of antifungal cyclic lipopeptides from cyanobacteria. Physiologia Plantarum 173: 639-650.
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237-240.
Finst RJ, Kim PJ, Quarmby LM. 1998. Genetics of the deflagellation pathway in Chlamydomonas. Genetics 149: 927-936.
Fricker MD, Plieth C, Knight H, Blancaflor E, Knight MR, White NS, Gilroy S. 1999. Fluorescence and luminescence techniques to probe ion activities in living plant cells. In: Mason WT, ed. Fluorescent and luminescent probes for biological activity. Amsterdam, the Netherlands: Elsevier, 569-596.
Fujiu K, Nakayama Y, Iida H, Sokabe M, Yoshimura K. 2011. Mechanoreception in motile flagella of Chlamydomonas. Nature Cell Biology 13: 630-632.
Götze S, Stallforth P. 2020. Structure, properties, and biological functions of nonribosomal lipopeptides from Pseudomonads. Natural Product Reports 37: 29-54.
Grein F, Müller A, Scherer KM, Liu X, Ludwig KC, Klöckner A, Strach M, Sahl H-G, Kubitscheck U, Schneider T. 2020. Ca2+-daptomycin targets cell wall biosynthesis by forming a tripartite complex with undecaprenyl-coupled intermediates and membrane lipids. Nature Communications 11: 1-11.
Gross H, Stockwell VO, Henkels MD, Nowak-Thompson B, Loper JE, Gerwick WH. 2007. The genomisotopic approach: a systematic method to isolate products of orphan biosynthetic gene clusters. Chemistry and Biology 14: 53-63.
Harris EH. 1989. The Chlamydomonas sourcebook. A comprehensive guide to biology and laboratory use. New York, NY, USA: Academic Press.
Hart PT, Kleijn LHJ, De Bruin G, Oppedijk SF, Kemmink J, Martin NI. 2014. A combined solid- and solution-phase approach provides convenient access to analogues of the calcium-dependent lipopeptide antibiotics. Organic and Biomolecular Chemistry 12: 913-918.
Hegemann P, Berthold P. 2009. Sensory photoreceptors and light control of flagellar activity. In: Harris EH, Stern DB, Witman GB, eds. The Chlamydomonas sourcebook, 2nd edn. New York, NY, USA: Academic Press, 395-429.
Hilton LK, Meili F, Buckoll PD, Rodriguez-Pike JC, Choutka CP, Kirschner JA, Warner F, Lethan M, Garces FA, Qi J et al. 2016. A forward genetic screen and whole genome sequencing identify deflagellation defective mutants in Chlamydomonas, including assignment of ADF1 as a TRP channel. G3 - Genes, Genomes, Genetics 6: 3409-3418.
Himmel NJ, Cox DN. 2020. Transient receptor potential channels: current perspectives on evolution, structure, function and nomenclature. Proceedings of the Royal Society B: Biological Sciences 287: 20201309.
Himmel NJ, Gray TR, Cox DN, Ruvinsky I. 2020. Phylogenetics identifies two eumetazoan TRPM clades and an eighth TRP family, TRP soromelastatin (TRPS). Molecular Biology and Evolution 37: 2034-2044.
Hom EFY, Aiyar P, Schaeme D, Mittag M, Sasso S. 2015. A chemical perspective on microalgal-microbial interactions. Trends in Plant Science 20: 689-693.
Hom EFY, Murray AW. 2014. Plant-fungal ecology. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science 345: 94-98.
Hotter V, Zopf D, Kim HJ, Silge A, Schmitt M, Aiyar P, Fleck J, Matthäus C, Hniopek J, Yan Q et al. 2021. A polyyne toxin produced by an antagonistic bacterium blinds and lyses a Chlamydomonad alga. Proceedings of the National Academy of Sciences, USA 118: e2107695118.
Huffer KE, Aleksandrova AA, Jara-Oseguera A, Forrest LR, Swartz KJ. 2020. Global alignment and assessment of TRP channel transmembrane domain structures to explore functional mechanisms. eLife 9: 1-33.
Ide T, Mochiji S, Ueki N, Yamaguchi K, Shigenobu S, Hirono M, Wakabayashi K. 2016. Identification of the agg1 mutation responsible for negative phototaxis in a “wild-type” strain of Chlamydomonas reinhardtii. Biochemistry and Biophysics Reports 7: 379-385.
Kaspar F, Neubauer P, Gimpel M. 2019. Bioactive secondary metabolites from Bacillus subtilis: a comprehensive review. Journal of Natural Products 82: 2038-2053.
Kozma MT, Schmidt M, Ngo-Vu H, Sparks SD, Senatore A, Derby CD. 2018. Chemoreceptor proteins in the Caribbean spiny lobster, Panulirus argus: expression of ionotropic receptors, gustatory receptors, and TRP channels in two chemosensory organs and brain. PLoS ONE 13: e0203935.
Krespach MKC, García-Altares M, Flak M, Schoeler H, Scherlach K, Netzker T, Schmalzl A, Mattern DJ, Schroeckh V, Komor A et al. 2020. Lichen-like association of Chlamydomonas reinhardtii and Aspergillus nidulans protects algal cells from bacteria. The ISME Journal 14: 2794-2805.
Lange M, Weihmann F, Schliebner I, Horbach R, Deising HB, Wirsel SGR, Peiter E. 2016. The transient receptor potential (TRP) channel family in Colletotrichum graminicola: a molecular and physiological analysis. PLoS ONE 11: e0158561.
Lazopulo S, Lazopulo A, Baker JD, Syed S. 2019. Daytime colour preference in Drosophila depends on the circadian clock and TRP channels. Nature 574: 108-111.
Li X, Patena W, Fauser F, Jinkerson RE, Saroussi S, Meyer MT, Ivanova N, Robertson JM, Yue R, Zhang R et al. 2019. A genome-wide algal mutant library and functional screen identifies genes required for eukaryotic photosynthesis. Nature Genetics 51: 627-635.
Li X, Zhang R, Patena W, Gang SS, Blum SR, Ivanova N, Yue R, Robertson JM, Lefebvre PA, Fitz-Gibbon ST et al. 2016. An indexed, mapped mutant library enables reverse genetics studies of biological processes in Chlamydomonas reinhardtii. Plant Cell 28: 367-387.
Lindström JB, Pierce NT, Latz MI. 2017. Role of TRP channels in dinoflagellate mechanotransduction. Biological Bulletin 233: 151-167.
Luxmi R, Kumar D, Mains RE, King SM, Eipper BA. 2019. Cilia-based peptidergic signaling. PLoS Biology 17: e3000566.
McGoldrick LL, Singh AK, Demirkhanyan L, Lin T-Y, Casner RG, Zakharian E, Sobolevsky AI. 2019. Structure of the thermo-sensitive TRP channel TRP1 from the alga Chlamydomonas reinhardtii. Nature Communications 10: 1-12.
Miller WR, Bayer AS, Arias CA. 2016. Mechanism of action and resistance to daptomycin in Staphylococcus aureus and enterococci. Cold Spring Harbor Perspectives in Medicine 6: a026997.
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R. 2020. IQ-Tree2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37: 1530-1534.
Müller A, Wenzel M, Strahl H, Grein F, Saaki TNV, Kohl B, Siersma T, Bandow JE, Sahl HG, Schneider T et al. 2016. Daptomycin inhibits cell envelope synthesis by interfering with fluid membrane microdomains. Proceedings of the National Academy of Sciences, USA 113: E7077-E7086.
Müller N, Wenzel S, Zou Y, Künzel S, Sasso S, Weiß D, Prager K, Grossman A, Kottke T, Mittag M. 2017. A plant cryptochrome controls key features of the Chlamydomonas circadian clock and its life cycle. Plant Physiology 174: 185-201.
Mullins AJ, Webster G, Kim HJ, Zhao J, Petrova YD, Ramming CE, Jenner M, Murray JAH, Connor TR, Hertweck C et al. 2021. Discovery of the Pseudomonas polyyne protegencin by a phylogeny-guided study of polyyne biosynthetic gene cluster diversity. mBio 12: e0071521.
Murata K, Suenaga M, Kai K. 2022. Genome mining discovery of protegenins A-D, bacterial polyynes involved in the antioomycete and biocontrol activities of Pseudomonas protegens. ACS Chemical Biology 17: 3313-3320.
Pazour GJ, Agrin N, Leszyk J, Witman GB. 2005. Proteomic analysis of a eukaryotic cilium. The Journal of Cell Biology 170: 103-113.
Pazour GJ, Witman GB. 2003. The vertebrate primary cilium is a sensory organelle. Current Opinion in Cell Biology 15: 105-110.
Peng G, Shi X, Kadowaki T. 2015. Evolution of TRP channels inferred by their classification in diverse animal species. Molecular Phylogenetics and Evolution 84: 145-157.
Petersen J, Rredhi A, Szyttenholm J, Mittag M. 2022. Evolution of circadian clocks along the green lineage. Plant Physiology 190: 924-937.
Quarmby LM, Hartzell HC. 1994. Two distinct, calcium-mediated, signal transduction pathways can trigger deflagellation in Chlamydomonas reinhardtii. The Journal of Cell Biology 124: 807-815.
Rose MM, Scheer D, Hou Y, Hotter VS, Komor AJ, Aiyar P, Scherlach K, Vergara F, Yan Q, Loper JE et al. 2021. The bacterium Pseudomonas protegens antagonizes the microalga Chlamydomonas reinhardtii using a blend of toxins. Environmental Microbiology 23: 5525-5540.
Saini HS, Barragán-Huerta BE, Lebrón-Paler A, Pemberton JE, Vázquez RR, Burns AM, Marron MT, Seliga CJ, Gunatilaka AAL, Maier RM. 2008. Efficient purification of the biosurfactant viscosin from Pseudomonas libanensis strain M9-3 and its physicochemical and biological properties. Journal of Natural Products 71: 1011-1015.
Salomé PA, Merchant SS. 2019. A series of fortunate events: introducing Chlamydomonas as a reference organism. Plant Cell 31: 1682-1707.
Sasso S, Stibor H, Mittag M, Grossman AR. 2018. From molecular manipulation of domesticated Chlamydomonas reinhardtii to survival in nature. eLife 7: e39233.
Stallforth P. 2020. Biosynthesis of bacterial natural products and small molecules in microbial interactions. Chembiochem 21: 2870.
Stallforth P, Mittag M, Brakhage AA, Hertweck C, Hellmich UA. 2023. Functional modulation of chemical mediators in microbial communities. Trends in Biochemical Sciences 48: 71-81.
Stewart AP, Smith GD, Sandford RN, Edwardson JM. 2010. Atomic force microscopy reveals the alternating subunit arrangement of the TRPP2-TRPV4 heterotetramer. Biophysical Journal 99: 790-797.
Verret F, Wheeler G, Taylor AR, Farnham G, Brownlee C. 2010. Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling. New Phytologist 187: 23-43.
Wada M, Kaizuka I, Yoshimura K. 2020. Responses to transient receptor potential (TRP) channel agonists in Chlamydomonas reinhardtii. Biology Open 9: bio053140.
Wang J, Barr MM. 2018. Cell-cell communication via ciliary extracellular vesicles: clues from model systems. Essays in Biochemistry 62: 205-213.
Wang J, Nikonorova I, Silva M, Walsh J, Tilton P, Gu A, Akella J, Barr MM. 2021. Sensory cilia act as a specialized venue for regulated extracellular vesicle biogenesis and signaling. Current Biology 31: 3943-3951.
Wu Q, Gao K, Zheng S, Zhu X, Liang Y, Pan J. 2018. Calmodulin regulates a TRP channel (ADF1) and phospholipase C (PLC) to mediate elevation of cytosolic calcium during acidic stress that induces deflagellation in Chlamydomonas. FASEB Journal 32: 3689-3699.
Xiu P, Liu R, Zhang D, Suna C. 2017. Pumilacidin-like lipopeptides derived from marine bacterium Bacillus sp. strain 176 suppress the motility of Vibrio alginolyticus. Applied and Environmental Microbiology 83: e00450-17.
Yu Z, Zhang T, Hao R, Zhu Y. 2019. Sensitivity of Chlamydomonas reinhardtii to cadmium stress is associated with phototaxis. Environmental Science: Processes & Impacts 21: 1011-1020.