Endogenous lipid chemoattractants and extracellular matrix proteins involved in development of Myxococcus xanthus

The soil bacterium Myxococcus xanthus is a model organism to study multicellular development and biofilm formation. When starved, swarms of M. xanthus cells aggregate into a multicellular architecture called a fruiting body, wherein cells differentiate into metabolically dormant myxospores. Fruiting body formation requires directed cell movement and production of an extracellular matrix (ECM) to facilitate cell-contact dependent motility (Social motility), and biofilm formation. M. xanthus displays chemotaxis towards phospholipids derived from its membrane containing the rare fatty acid 16:15c. This study demonstrates that 16:15c is primarily found at the sn-1 position within the major membrane phospholipid, phosphatidylethanolamine (PE), which is contrary to the established dogma of fatty acid localization in Gram-negative bacteria. Additionally, 16:15c at the sn-1 position stimulates chemotaxis stronger than 16:15c located at the sn-2 position. These results suggest that the endogenous lipid chemoattractants may serve as a self-recognition system. Chemotaxis towards a self-recognition marker could facilitate movement of cells into aggregation centers. Lipid chemotaxis is dependent on the ECM-associated zinc metalloprotease FibA, suggesting that the ECM may harbor protein components of extracellular signaling pathways. Protein componentsof prokaryotic biofilms are largely unexplored. Twenty one putative ECM-associated proteins were identified, including FibA. Many are novel proteins. A large portion of the putative ECM proteins have lipoprotein secretion signals, unusual for extracellular proteins. An MXAN4860 pilA mutant displays a 24 hour delay in fruiting body formation and sporulation compared to the pilA parent, indicating that MXAN4860 functions in the FibA-mediated developmental pathway previously described. The ECM provides the main connective network between cells in fruiting bodies and biofilms, and the proteins identified here may be components of novel signaling pathways controlling communal cellular behavior.