Abstract
The Type VI Secretion System (T6SS) functions in bacteria as a contractile nanomachine that punctures and delivers lethal effectors to a target cell. Virtually nothing is known about the lifestyle or physiology that dictates when bacteria normally produce their T6SS, which prevents a clear understanding of how bacteria benefit from its action in their natural habitat. Proteus mirabilis undergoes a characteristic developmental process to coordinate a multicellular swarming behavior and will discriminate itself from another Proteus isolate during swarming, resulting in a visible boundary termed a Dienes line. Using transposon mutagenesis, we discovered that this recognition phenomenon requires the lethal action of the T6SS. All mutants identified in the genetic screen had insertions within a single 33.5-kb region that encodes a T6SS and cognate Hcp-VrgG-linked effectors. The identified T6SS and primary effector operons were characterized by killing assays, by construction of additional mutants, by complementation, and by examining the activity of the type VI secretion system in real-time using live-cell microscopy on opposing swarms. We show that lethal T6SS-dependent activity occurs when a dominant strain infiltrates deeply beyond the boundary of the two swarms. Using this multicellular model, we found that social recognition in bacteria, underlying killing, and immunity to killing all require cell-cell contact, can be assigned to specific genes, and are dependent on the T6SS. The ability to survive a lethal T6SS attack equates to “recognition”. In contrast to the current model of T6SS being an offensive or defensive weapon our findings support a preemptive mechanism by which an entire population indiscriminately uses the T6SS for contact-dependent delivery of effectors during its cooperative mode of growth.
Highlights
The type VI secretion system (T6SS), a recently discovered Gram-negative secretion pathway [1,2], delivers effectors upon direct contact with a target cell [3,4] through a contractile puncturing device
Death of the target cell is the primary outcome that follows the delivery of the lethal effectors, which are translocated from the attacker cell cytoplasm into the periplasm of the target cell via a T6S apparatus in a contact-dependent process [5,6]
Little is known about the lifestyle or physiology dictating when bacteria normally express their T6SS
Summary
The type VI secretion system (T6SS), a recently discovered Gram-negative secretion pathway [1,2], delivers effectors upon direct contact with a target cell [3,4] through a contractile puncturing device. We would expect bacteria that have developed multicellular behavior to benefit from a mechanism that depends on cell-cell contact to discriminate between one another and eliminate non-self bacteria, potential cheaters, or competitors from the population. In this regard, T6SS activity, like multicellular behavior, requires direct cell-cell contact. Lethal action of the T6SS would provide a specific advantage for bacteria to discriminate, recognize, and kill competitors that would otherwise interfere or benefit from a cooperative behavior. Despite the strict requirement for cell-cell contact to achieve multicellular behavior and direct contact being required to trigger the contractile T6SS, any relationship between the two remains an open question [8]
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