Cyanobacterial biofilms are ubiquitous and play important roles in diverse environments, yet, understanding of the processes underlying the development of these aggregates is just emerging. Here we report cell specialization in formation of Synechococcus elongatus PCC 7942 biofilms—a hitherto unknown characteristic of cyanobacterial social behavior. We show that only a quarter of the cell population expresses at high levels the four-gene ebfG-operon that is required for biofilm formation. Almost all cells, however, are assembled in the biofilm. Detailed characterization of EbfG4 encoded by this operon revealed cell-surface localization as well as its presence in the biofilm matrix. Moreover, EbfG1-3 were shown to form amyloid structures such as fibrils and are thus likely to contribute to the matrix structure. These data suggest a beneficial ‘division of labor’ during biofilm formation where only some of the cells allocate resources to produce matrix proteins—‘public goods’ that support robust biofilm development by the majority of the cells. In addition, previous studies revealed the operation of a self-suppression mechanism that depends on an extracellular inhibitor, which supresses transcription of the ebfG-operon. Here we revealed inhibitor activity at an early growth stage and its gradual accumulation along the exponential growth phase in correlation with cell density. Data, however, do not support a threshold-like phenomenon known for quorum-sensing in heterotrophs. Together, data presented here demonstrate cell specialization and imply density-dependent regulation thereby providing deep insights into cyanobacterial communal behavior.
Bibliographical noteFunding Information:
We thank Ryan Simkovsky for providing the vector for EbfG4-tagging. Studies in the laboratories of Rakefet Schwarz and Susan Golden were supported by the program of the National Science Foundation and the US-Israel Binational Science Foundation (NSF-BSF 2012823). This study was also supported by grants from the Israel Science Foundation (ISF 1406/14 and 2494/19) to Rakefet Schwarz. Studies in the laboratory of Eric Kemen were supported by the graduate school GRK 1708 “Molecular principles of bacterial survival strategies” and the European Research Council (ERC) under the DeCoCt research program (grant agreement: ERC-2018-COG 820124).
© 2023, The Author(s).