in

Lichen-like association of Chlamydomonas reinhardtii and Aspergillus nidulans protects algal cells from bacteria

  • 1.

    Taylor TN, Remy W, Hass H. Parasitism in a 400-million-year-old green alga. Nature. 1992;357:493–4.

    Google Scholar 

  • 2.

    Taylor TN, Hass H, Remy W, Kerp H. The oldest fossil lichen. Nature. 1995;378:244.

    CAS  Google Scholar 

  • 3.

    Honegger R, Edwards D, Axe L. The earliest records of internally stratified cyanobacterial and algal lichens from the lower devonian of the welsh borderland. N Phytol. 2013;197:264–75.

    Google Scholar 

  • 4.

    Selosse MA, Le Tacon F. The land flora: a phototroph-fungus partnership?. Trends Ecol Evol. 1998;13:15–20.

    CAS  PubMed  Google Scholar 

  • 5.

    Schwendener S. Die Algentypen der Flechtengonidien. Universitätsbuchdruckerei von C Schultze, Basel. 1869.

  • 6.

    Ahmadjian V, Jacobs JB. Relationship between fungus and alga in the lichen Cladonia cristatella Tuck. Nature. 1981;289:169–72.

    Google Scholar 

  • 7.

    Brakhage AA. Regulation of fungal secondary metabolism. Nat Rev Microbiol. 2013;11:21–32.

    CAS  PubMed  Google Scholar 

  • 8.

    Netzker T, Fischer J, Weber J, Mattern DJ, König CC, Valiante V, et al. Microbial communication leading to the activation of silent fungal secondary metabolite gene clusters. Front Microbiol. 2015;6:299.

    PubMed  PubMed Central  Google Scholar 

  • 9.

    Grube M, Cernava T, Soh J, Fuchs S, Aschenbrenner I, Lassek C, et al. Exploring functional contexts of symbiotic sustain within lichen-associated bacteria by comparative omics. ISME J. 2015;9:412–24.

    CAS  PubMed  Google Scholar 

  • 10.

    Grube M, Cardinale M, de Castro JV Jr, Müller H, Berg G. Species-specific structural and functional diversity of bacterial communities in lichen symbioses. ISME J. 2009;3:1105.

    PubMed  Google Scholar 

  • 11.

    Schneider O, Simic N, Aachmann FL, Rückert C, Kristiansen KA, Kalinowski J, et al. Genome mining of Streptomyces sp. YIM 130001 isolated from lichen affords new thiopeptide antibiotic. Front Microbiol. 2018;9:3139.

    PubMed  PubMed Central  Google Scholar 

  • 12.

    Liu C, Jiang Y, Lei H, Chen X, Ma Q, Han L, et al. Four new nanaomycins produced by Streptomyces hebeiensis derived from lichen. Chem Biodivers. 2017;14:e1700057.

    Google Scholar 

  • 13.

    Parrot D, Antony-Babu S, Intertaglia L, Grube M, Tomasi S, Suzuki MT. Littoral lichens as a novel source of potentially bioactive Actinobacteria. Sci Rep. 2015;5:15839.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 14.

    Parrot D, Legrave N, Delmail D, Grube M, Suzuki M, Tomasi S. Review—Lichen-associated bacteria as a hot spot of chemodiversity: Focus on uncialamycin, a promising compound for future medicinal applications. Planta Med. 2016;82:1143–52.

    CAS  PubMed  Google Scholar 

  • 15.

    Netzker T, Flak M, Krespach MKC, Stroe MC, Weber J, Schroeckh V, et al. Microbial interactions trigger the production of antibiotics. Curr Opin Microbiol. 2018;45:117–23.

    CAS  PubMed  Google Scholar 

  • 16.

    Fischer J, Müller SY, Netzker T, Jäger N, Gacek-Matthews A, Scherlach K, et al. Chromatin mapping identifies BasR, a key regulator of bacteria-triggered production of fungal secondary metabolites. eLife. 2018;7:e40969.

    PubMed  PubMed Central  Google Scholar 

  • 17.

    Schroeckh V, Scherlach K, Nützmann HW, Shelest E, Schmidt-Heck W, Schuemann J, et al. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA. 2009;106:14558–63.

    CAS  PubMed  Google Scholar 

  • 18.

    Stöcker-Worgötter E. Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep. 2008;25:188–200.

    PubMed  Google Scholar 

  • 19.

    Hom EFY, Murray AW. Niche engineering demonstrates a latent capacity for fungal-algal mutualism. Science. 2014;345:94–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 20.

    Netzker T, Schroeckh V, Gregory MA, Flak M, Krespach MKC, Leadlay PF, et al. An efficient method to generate gene deletion mutants of the rapamycin-producing bacterium Streptomyces iranensis HM 35. Appl Environ Microbiol. 2016;82:3481–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 21.

    Xu W, Zhai G, Liu Y, Li Y, Shi Y, Hong K, et al. An iterative module in the azalomycin F polyketide synthase contains a switchable enoylreductase domain. Angew Chem Int Ed. 2017;56:5503–6.

    CAS  Google Scholar 

  • 22.

    Gorman D, Levine R. Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Proc Natl Acad Sci USA. 1965;54:1665–9.

    CAS  PubMed  Google Scholar 

  • 23.

    Sjoblad RD, Frederikse PH. Chemotactic responses of Chlamydomonas reinhardtii. Mol Cell Biol. 1981;1:1057–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 24.

    Kessler RW, Weiss A, Kuegler S, Hermes C, Wichard T. Macroalgal-bacterial interactions: Role of dimethylsulfoniopropionate in microbial gardening by Ulva (Chlorophyta). Mol Ecol. 2018;27:1808–19.

    CAS  PubMed  Google Scholar 

  • 25.

    Paul C, Mausz MA, Pohnert G. A co-culturing/metabolomics approach to investigate chemically mediated interactions of planktonic organisms reveals influence of bacteria on diatom metabolism. Metabolomics. 2013;9:349–59.

    CAS  Google Scholar 

  • 26.

    Xu L, Xu X, Yuan G, Wang Y, Qu Y, Liu E. Mechanism of azalomycin F5a against methicillin-resistant Staphylococcus aureus. BioMed Res Int. 2018;2018:6942452.

    PubMed  PubMed Central  Google Scholar 

  • 27.

    Pouneva I. Evaluation of algal viability and physiology state by fluorescent microscopic methods. Bulgarian J Plant Physiol. 1997;23:67–76.

    Google Scholar 

  • 28.

    Blin K, Wolf T, Chevrette MG, Lu X, Schwalen CJ, Kautsar SA, et al. antiSMASH 4.0—improvements in chemistry prediction and gene cluster boundary identification. Nucleic Acids Res. 2017;45:W36–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 29.

    Arai M. Azalomycin F, an antibiotic against fungi and Trichomonas. Arzneimittelforschung. 1968;18:1396–9.

    CAS  PubMed  Google Scholar 

  • 30.

    Hong H, Sun Y, Zhou Y, Stephens E, Samborskyy M, Leadlay PF. Evidence for an iterative module in chain elongation on the azalomycin polyketide synthase. Beilstein J Org Chem. 2016;12:2164–72.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 31.

    Yuan GJ, Li PB, Yang J, Pang HZ, Pei Y. Anti-methicillin-resistant Staphylococcus aureus assay of azalomycin F5a and its derivatives. Chin J Nat Med. 2014;12:309–13.

    CAS  PubMed  Google Scholar 

  • 32.

    Hong H, Fill T, Leadlay PF. A common origin for guanidinobutanoate starter units in antifungal natural products. Angew Chem Int Ed. 2013;52:13096–9.

    CAS  Google Scholar 

  • 33.

    Bennoun P, Spierer-Herz M, Erickson J, Girard-Bascou J, Pierre Y, Delosme M, et al. Characterization of photosystem II mutants of Chlamydomonas reinhardii lacking the psbA gene. Plant Mol Biol. 1986;6:151–60.

    CAS  PubMed  Google Scholar 

  • 34.

    Erickson JM, Rahire M, Malnoë P, Girard-Bascou J, Pierre Y, Bennoun P, et al. Lack of the D2 protein in a Chlamydomonas reinhardtii psbD mutant affects photosystem II stability and D1 expression. EMBO J. 1986;5:1745–54.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 35.

    Masloff S, Pöggeler S, Kück U. The pro1 + gene from Sordaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics. 1999;152:191–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 36.

    Yuan G, Xu L, Xu X, Li P, Zhong Q, Xia H, et al. Azalomycin F5a, a polyhydroxy macrolide binding to the polar head of phospholipid and targeting to lipoteichoic acid to kill methicillin-resistant Staphylococcus aureus. Biomed Pharmacother. 2019;109:1940–50.

    CAS  PubMed  Google Scholar 

  • 37.

    Cheng J, Yang SH, Palaniyandi SA, Han JS, Yoon T-M, Kim T-J, et al. Azalomycin F complex is an antifungal substance produced by Streptomyces malaysiensis MJM1968 isolated from agricultural soil. J Korean Soc Appl Biol Chem. 2010;53:545–52.

    CAS  Google Scholar 

  • 38.

    Du ZY, Alvaro J, Hyden B, Zienkiewicz K, Benning N, Zienkiewicz A, et al. Enhancing oil production and harvest by combining the marine alga Nannochloropsis oceanica and the oleaginous fungus Mortierella elongata. Biotechnol Biofuels. 2018;11:174.

    PubMed  PubMed Central  Google Scholar 

  • 39.

    Du ZY, Zienkiewicz K, Vande Pol N, Ostrom NE, Benning C, Bonito GM. Algal-fungal symbiosis leads to photosynthetic mycelium. eLife. 2019;8:e47815.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 40.

    Muggia L, Fernández-Brime S, Grube M, Wedin M. Schizoxylon as an experimental model for studying interkingdom symbiosis. FEMS Microbiol Ecol. 2016;92:fiw165.

    PubMed  Google Scholar 

  • 41.

    Grube M, Wedin M. Lichenized fungi and the evolution of symbiotic organization. Microbiol Spectr. 2016;4.

  • 42.

    Aschenbrenner IA, Cernava T, Berg G, Grube M. Understanding microbial multi-species symbioses. Front Microbiol. 2016;7:180.

    PubMed  PubMed Central  Google Scholar 

  • 43.

    Gershenzon J, Dudareva N. The function of terpene natural products in the natural world. Nat Chem Biol. 2007;3:408–14.

    CAS  PubMed  Google Scholar 

  • 44.

    Shabuer G, Ishida K, Pidot SJ, Roth M, Dahse H-M, Hertweck C. Plant pathogenic anaerobic bacteria use aromatic polyketides to access aerobic territory. Science. 2015;350:670–4.

    CAS  PubMed  Google Scholar 

  • 45.

    Kinsinger RF, Shirk MC, Fall R. Rapid surface motility in Bacillus subtilis is dependent on extracellular surfactin and potassium ion. J Bacteriol. 2003;185:5627–31.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 46.

    Aiyar P, Schaeme D, García-Altares M, Carrasco Flores D, Dathe H, Hertweck C, et al. Antagonistic bacteria disrupt calcium homeostasis and immobilize algal cells. Nat Commun. 2017;8:1756.

    PubMed  PubMed Central  Google Scholar 

  • 47.

    Stroe MC, Netzker T, Scherlach K, Krüger T, Hertweck C, Valiante V, et al. Targeted induction of a silent fungal gene cluster encoding the bacteria-specific germination inhibitor fumigermin. eLife. 2020;9:e52541.

    PubMed  PubMed Central  Google Scholar 

  • 48.

    Harvey BM, Mironenko T, Sun Y, Hong H, Deng Z, Leadlay PF, et al. Insights into polyether biosynthesis from analysis of the nigericin biosynthetic gene cluster in Streptomyces sp. DSM4137. Cell Chem Biol. 2007;14:703–14.

    CAS  Google Scholar 

  • 49.

    Zheng X, Zhang B, Zhang J, Huang L, Lin J, Li X, et al. A marine algicidal actinomycete and its active substance against the harmful algal bloom species Phaeocystis globosa. Appl Microbiol Biotechnol. 2013;97:9207–15.

    CAS  PubMed  Google Scholar 

  • 50.

    Greiner A, Kelterborn S, Evers H, Kreimer G, Sizova I, Hegemann P. Targeting of photoreceptor genes in Chlamydomonas reinhardtii via zinc-finger nucleases and CRISPR/Cas9. Plant Cell. 2017;29:2498–518.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 51.

    Le TB, Fiedler HP, den Hengst CD, Ahn SK, Maxwell A, Buttner MJ. Coupling of the biosynthesis and export of the DNA gyrase inhibitor simocyclinone in Streptomyces antibioticus. Mol Microbiol. 2009;72:1462–74.

    CAS  PubMed  Google Scholar 

  • 52.

    Xu Y, Willems A, Au-Yeung C, Tahlan K, Nodwell JR. A two-step mechanism for the activation of actinorhodin export and resistance in Streptomyces coelicolor. MBio. 2012;3:e00191–12.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 53.

    Wymann MP, Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim Biophys Acta. 1998;1436:127–50.

    CAS  PubMed  Google Scholar 

  • 54.

    Vanzela AP, Said S, Prade RA. Phosphatidylinositol phospholipase C mediates carbon sensing and vegetative nuclear duplication rates in Aspergillus nidulans. Can J Microbiol. 2011;57:611–6.

    PubMed  Google Scholar 

  • 55.

    Schink KO, Tan KW, Stenmark H. Phosphoinositides in control of membrane dynamics. Annu Rev Cell Dev Biol. 2016;32:143–71.

    CAS  PubMed  Google Scholar 

  • 56.

    Miller MB, Haubrich BA, Wang Q, Snell WJ, Nes WD. Evolutionarily conserved Δ25(27)-olefin ergosterol biosynthesis pathway in the alga Chlamydomonas reinhardtii. J Lipid Res. 2012;53:1636–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 57.

    Shapiro BE, Gealt MA. Ergosterol and lanosterol from Aspergillus nidulans. Microbiology. 1982;128:1053–6.

    CAS  Google Scholar 

  • 58.

    Anderson TM, Clay MC, Cioffi AG, Diaz KA, Hisao GS, Tuttle MD, et al. Amphotericin forms an extramembranous and fungicidal sterol sponge. Nat Chem Biol. 2014;10:400–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 59.

    Laterre P-F, Colin G, Dequin P-F, Dugernier T, Boulain T, Azeredo da Silveira S, et al. CAL02, a novel antitoxin liposomal agent, in severe pneumococcal pneumonia: a first-in-human, double-blind, placebo-controlled, randomised trial. Lancet Infect Dis. 2019;19:620–30.

    CAS  PubMed  Google Scholar 

  • 60.

    Pletz MW, Bauer M, Brakhage AA. One step closer to precision medicine for infectious diseases. Lancet Infect Dis. 2019;19:564–5.

    PubMed  Google Scholar 

  • 61.

    Miransari M. Arbuscular mycorrhizal fungi and nitrogen uptake. Arch Microbiol. 2011;193:77–81.

    CAS  PubMed  Google Scholar 

  • 62.

    Otto S, Bruni EP, Harms H, Wick LY. Catch me if you can: dispersal and foraging of Bdellovibrio bacteriovorus 109J along mycelia. ISME J. 2017;11:386–93.

    PubMed  Google Scholar 

  • 63.

    Pion M, Spangenberg JE, Simon A, Bindschedler S, Flury C, Chatelain A, et al. Bacterial farming by the fungus Morchella crassipes. Proc R Soc B Biol Sci. 2013;280:20132242.

    Google Scholar 

  • 64.

    Splivallo R, Deveau A, Valdez N, Kirchhoff N, Frey-Klett P, Karlovsky P. Bacteria associated with truffle-fruiting bodies contribute to truffle aroma. Environ Microbiol. 2015;17:2647–60.

    PubMed  Google Scholar 

  • 65.

    Lutzoni F, Pagel M, Reeb V. Major fungal lineages are derived from lichen symbiotic ancestors. Nature. 2001;411:937–40.

    CAS  PubMed  Google Scholar 

  • 66.

    Mukhin VA, Patova EN, Kiseleva IS, Neustroeva NV, Novakovskaya IV. Mycetobiont symbiotic algae of wood-decomposing fungi. Russ J Ecol. 2016;47:133–7.

    CAS  Google Scholar 

  • 67.

    Delaux P-M, Radhakrishnan GV, Jayaraman D, Cheema J, Malbreil M, Volkening JD, et al. Algal ancestor of land plants was preadapted for symbiosis. Proc Natl Acad Sci USA. 2015;112:13390–5.

    CAS  PubMed  Google Scholar 

  • 68.

    Lutzoni F, Nowak MD, Alfaro ME, Reeb V, Miadlikowska J, Krug M, et al. Contemporaneous radiations of fungi and plants linked to symbiosis. Nat Commun. 2018;9:5451.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 69.

    Kranner I, Cram WJ, Zorn M, Wornik S, Yoshimura I, Stabentheiner E, et al. Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc Natl Acad Sci USA. 2005;102:3141–6.

    CAS  PubMed  Google Scholar 

  • 70.

    Larson DW. Lichen water relations under drying conditions. N Phytol. 1979;82:713–31.

    Google Scholar 


  • Source: Ecology - nature.com

    Author Correction: Political dynamics and governance of World Heritage ecosystems

    Special issue: Biofunctional gels