Claessen, D.

Dijkhuizen, L.

van Keulen, G

Wosten, H.A B

English

Proceedings - University of Groningen

   University of GroningenStreptomyces coelicolor in an oxygen-limited liquid environment: adapt and escapeClaessen, D.; Wosten, H.A B; Dijkhuizen, L.; van Keulen, GPublished in:Microbiology AustraliaIMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite fromit. Please check the document version below.Document VersionPublisher's PDF, also known as Version of recordPublication date:2004Link to publication in University of Groningen/UMCG research databaseCitation for published version (APA):Claessen, D., Wosten, H. A. B., Dijkhuizen, L., & van Keulen, G. (2004). Streptomyces coelicolor in anoxygen-limited liquid environment: adapt and escape. Microbiology Australia, 25(2), 22 - 23.CopyrightOther than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of theauthor(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).The publication may also be distributed here under the terms of Article 25fa of the Dutch Copyright Act, indicated by the “Taverne” license.More information can be found on the University of Groningen website: https://www.rug.nl/library/open-access/self-archiving-pure/taverne-amendment.Take-down policyIf you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediatelyand investigate your claim.Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum.Download date: 02-06-202222 M I C R O B I O L O G Y  A U S T R A L I A  •  M A Y  2 0 0 4Under the MicroscopeIntroductionStreptomycetes are mycelial soil bacteriathat undergo a complex developmentalcycle on solid media.  Spores germinateand form a branched, vegetativemycelium.  Several signals trigger the formation ofhydrophobic aerial hyphae thatdifferentiate further into reproductivechains of spores.  Differentiation isaccompanied by the production ofsecondary metabolites, e.g. antibiotics.  We have studied the development ofStreptomyces coelicolor in standing liquidcultures.  The media in these culturesshow steep oxygen gradients 1 which aresimilar to those found in flooded soils.For example, nutrient rich media werealready anoxic 1-2mm below the surface.How does S. coelicolor cope with this?Recent research indicates that thisbacterium adapts and escapes.Despite the oxygen limitation in thestanding liquid cultures, S. coelicolorreadily colonised the medium (Figure 1),implying the presence of an activeanaerobic metabolism 1.  Growth of S.coelicolor under anaerobic conditionshad not been reported before.  Yet,various genes within the genome arepredicted to be involved in low oxygenstress, nitrate and nitrite respiration, andfermentation (http://www.sanger.ac.uk/Projects/S_coelicolor/).  This indicatesthat this bacterium is fully equipped togrow under these conditions.  Hyphae in the aqueous anaerobicenvironment not only grow freely in themedium but also attach to and grow overthe hydrophobic surface of the well(Figure 1) 1, 2.  Attachment of hyphae wasreduced in strains in which the rdlA andrdlB genes had been deleted.  Thesegenes encode for homologous secretedproteins called rodlins.  Rodlins are onlyproduced by hyphae in contact with ahydrophobic environment such as ahydrophobic solid or the air and form (orare part of) a rodlet-decorated outer cellwall layer (Figure 2).  The finding that the rdl genes are notonly expressed under aerobic conditions,but also in oxygen-limited conditions,suggests that regulation of these genesand possibly other developmentallyregulated genes as well, is not signalledthrough oxygen levels.  After a period of submerged growth,hyphae in the liquid standing culturemigrated to the air interface (Figure 1) 1.How hyphae move to this interface iscurrently being studied.  Possibly,buoyancy of S. coelicolor is provided bythe formation of gas vesicles encoded forby two gas vesicle gene clusters that arecontained in the genome.  Hyphae inshaken liquid cultures do not float whenthese cultures are no longer shakenwhich indicates that shear forces mayhave a negative effect on flotation.  The observed decrease in oxygen tensionand nutrient limitation in standing liquidcultures could form additional triggers forbecoming buoyant.  At the air interfacefloating colonies were formed thatproduced sporulating aerial hyphae(Figure 1) similar to those on solid agarmedia.  Interestingly, the floating colonieswere fixed at the air interface by a rigidlight reflecting film.  However, this filmdoes not seem to be involved in enablinghyphae to escape the water to grow intothe air.  This was concluded from a recentstudy showing that chaplins(hydrophobic cell surface proteinsinvolved in aerial mycelium formation)fulfil this function.  A strain in which six out of eight chaplinsgenes were deleted was strongly affectedin its formation of aerial hyphae 3, 4.However, the light reflecting film was stillformed 3.  Aerial growth on solid mediumcould be restored in the mutant byapplying purified chaplins to the colonysurface 3, indicating that chaplins mightact as surfactants.  Indeed, mixtures ofchaplins were shown to lower the watersurface tension from 72-28mJ m-2.  This surface activity is accompanied bymajor conformational changes in theproteins.  At the water-air interface,chaplins assemble into small amyloid-likefibrils that are rich in ß-sheet 3.  Chaplinsare the first reported example offunctional amyloid-like proteins in Gram-positive bacteria and only the second inthe prokaryotic domains.  Future research will focus on metabolismunder oxygen limited conditions and onthe role of the light reflecting film formedat the water-air interface.  Identification ofthe molecules that make up this film willbe the first step.Streptomyces coelicolor in an oxygen-limited liquid environment: adapt and escapeDennis ClaessenHan AB WöstenLubbert DijkhuizenGeertje van KeulenUniversity of GroningenDepartment of MicrobiologyKerklaan 309751 NN HarlenThe NetherlandsTel: (31) 50 3632160Fax: (31) 50 3632154E-mail: D.Claessen@biol.rug.nlM I C R O B I O L O G Y  A U S T R A L I A  •  M A Y  2 0 0 4 23Under the MicroscopeDC and GVK are supported by a grant ofthe Dutch Programme EET (Economy,Ecology and Technology: EETK01031).References1. van Keulen G, Jonkers HM, Claessen D,Dijkhuizen L & Wösten HAB.  Differentiation andanaerobiosis in standing liquid cultures ofStreptomyces coelicolor.  J. Bacteriol. 2003;185:1455-1458.2. Claessen D, Wösten HAB, van Keulen G, FaberOG, Alves AMCR, Meijer WG & Dijkhuizen L.  Twonovel homologous proteins of Streptomycescoelicolor and Streptomyces lividans areinvolved in the formation of the rodlet layer andmediate attachment to a hydrophobic solid.  Mol.Microbiol. 2002; 44:1483-1492.3. Claessen D, Rink R, de Jong W, Siebring J, deVreugd P, Boersma FGH, Dijkhuizen L & WöstenHAB.  A novel class of secreted hydrophobicproteins is involved in aerial hyphae formation inStreptomyces coelicolor by forming amyloid-likefibrils. Genes Dev. 2003; 17:1714-1726.4. Elliot MA, Karoonuthaisiri N, Huang J, Bibb MJ,Cohen SN, Kao CM & Buttner MJ.  The chaplins:a family of hydrophobic cell-surface proteinsinvolved in aerial mycelium formation inStreptomyces coelicolor.  Genes Dev. 2003;17:1727-1740.Figure 2. The outer surface of aerial structures of S. coelicolor is characterised bya typical ultrastructure called the rodlet layer.Figure 1. Standing liquid cultures of S. coelicolor demonstrate an extended life cycle, attachment to hydrophobic solids andnovel metabolic pathways.

Streptomyces coelicolor in an oxygen-limited liquid environment: adapt and escape

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Streptomyces coelicolor in an oxygen-limited liquid environment: adapt and escape

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