Cross-membranes orchestrate compartmentalization and morphogenesis in Streptomyces.
Far from being simple unicellular entities, bacteria have complex social behaviour and organization, living in large populations, and some even as coherent, multicellular entities. The filamentous streptomycetes epitomize such multicellularity, growing as a syncytial mycelium with physiologically distinct hyphal compartments separated by infrequent cross-walls. The viability of mutants devoid of cell division, which can be propagated from fragments, suggests the presence of a different form of compartmentalization in the mycelium. Here we show that complex membranes, visualized by cryo-correlative light microscopy and electron tomography, fulfil this role. Membranes form small assemblies between the cell wall and cytoplasmic membrane, or, as evidenced by FRAP experiments, large protein-impermeable cross-membrane structures, which compartmentalize the multinucleoid mycelium. All areas containing cross-membrane structures are nucleoid-restricted zones, suggesting that the membrane assemblies may also act to protect nucleoids from cell-wall restructuring events. Our work reveals a novel mechanism of controlling compartmentalization and development in multicellular bacteria.
Department of Molecular Biotechnology, Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 AB Leiden, The Netherlands.
Katherine
K
Celler
Department of Molecular Cell Biology, Leiden University Medical Centre, PO Box 9600, 2300 RC Leiden, The Netherlands.
Roman I
0000-0001-6736-7147
RI
Koning
Department of Molecular Biotechnology, Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 AB Leiden, The Netherlands.
Joost
J
Willemse
Department of Molecular Cell Biology, Leiden University Medical Centre, PO Box 9600, 2300 RC Leiden, The Netherlands.
Abraham J
AJ
Koster
Department of Molecular Biotechnology, Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 AB Leiden, The Netherlands.
Gilles P
0000-0003-0341-1561
GP
van Wezel
D001426:Bacterial Proteins / Q000378:metabolism; D001896:Boron Compounds; D002451:Cell Compartmentation; D002462:Cell Membrane / Q000187:drug effects / Q000378:metabolism*; D002473:Cell Wall / Q000187:drug effects / Q000378:metabolism; D002876:Chromosomes, Bacterial / Q000378:metabolism; D004269:DNA, Bacterial / Q000378:metabolism; D055032:Electron Microscope Tomography; D036681:Fluorescence Recovery After Photobleaching; D025301:Hyphae / Q000187:drug effects / Q000378:metabolism; D009024:Morphogenesis / Q000187:drug effects; D013194:Staining and Labeling; D013302:Streptomyces / Q000187:drug effects / Q000254:growth & development* / Q000378:metabolism; D014640:Vancomycin / Q000494:pharmacology
C095489:4,4-difluoro-4-bora-3a,4a-diaza-s-indacene; D001426:Bacterial Proteins; D001896:Boron Compounds; D004269:DNA, Bacterial; D014640:Vancomycin