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Trade-offs constrain adaptive pathways to the type VI secretion system survival.

ABSTRACT: The Type VI Secretion System (T6SS) is a nano-harpoon used by many bacteria to inject toxins into neighboring cells. While much is understood about mechanisms of T6SS-mediated toxicity, less is known about the ways that competitors can defend themselves against this attack, especially in the absence of their own T6SS. Here we subjected eight replicate populations of Escherichia coli to T6SS attack by Vibrio cholerae. Over ∼500 generations of competition, isolates of the E. coli populations evolved to survive T6SS attack an average of 27-fold better, through two convergently evolved pathways: apaH was mutated in six of the eight replicate populations, while the other two populations each had mutations in both yejM and yjeP. However, the mutations we identified are pleiotropic, reducing cellular growth rates, and increasing susceptibility to antibiotics and elevated pH. These trade-offs help us understand how the T6SS shapes the evolution of bacterial interactions.

SUBMITTER: MacGillivray KA

PROVIDER: S-EPMC10679819 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Trade-offs constrain adaptive pathways to the type VI secretion system survival.

MacGillivray Kathryn A KA Ng Siu Lung SL Wiesenfeld Sophia S Guest Randi L RL Jubery Tahrima T Silhavy Thomas J TJ Ratcliff William C WC Hammer Brian K BK

iScience 20231026 12

The Type VI Secretion System (T6SS) is a nano-harpoon used by many bacteria to inject toxins into neighboring cells. While much is understood about mechanisms of T6SS-mediated toxicity, less is known about the ways that competitors can defend themselves against this attack, especially in the absence of their own T6SS. Here we subjected eight replicate populations of Escherichia coli to T6SS attack by Vibrio cholerae. Over ∼500 generations of competition, isolates of the E. coli< ...[more]

PMID: 38025790

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Project description:The bacterium Proteus mirabilis can communicate identity through the secretion of the self-identity protein IdsD via the type VI secretion (T6S) system. IdsD secretion is essential for self-versus-nonself recognition behaviors in these populations. Here we provide an answer to the unresolved question of how the activity of a T6S substrate, such as IdsD, is regulated before secretion. We demonstrate that IdsD is found in clusters that form independently of the T6S machinery and activity. We show that the IdsC protein, which is a member of the proposed DUF4123 chaperone family, is essential for the maintenance of these clusters and of the IdsD protein itself. We provide evidence that amino acid disruptions in IdsC are sufficient to disrupt IdsD secretion but not IdsD localization into subcellular clusters, strongly supporting the notion that IdsC functions in at least two different ways: maintaining IdsD levels and secreting IdsD. We propose that IdsC, and likely other DUF4123-containing proteins, functions to regulate T6S substrates in the donor cell both by maintaining protein levels and by mediating secretion at the T6S machinery.IMPORTANCE Understanding the subcellular dynamics of self-identity proteins is crucial for developing models of self-versus-nonself recognition. We directly addressed how a bacterium restricts self-identity information before cell-cell exchange. We resolved two conflicting models for type VI secretion (T6S) substrate regulation by focusing on the self-identity protein IdsD. One model is that a cognate immunity protein binds the substrate, inhibiting activity before transport. Another model proposes that DUF4123 proteins act as chaperones in the donor cell, but no detailed molecular mechanism was previously known. We resolve this discrepancy and propose a model wherein a chaperone couples IdsD sequestration with its localization. Such a molecular mechanism restricts the communication of identity, and possibly other T6S substrates, in producing cells.

Project description:The type VI secretion system (T6SS) is used by many Gram-negative bacteria to deploy toxic effectors for interbacterial competition. This system provides a competitive advantage in planta to agrobacteria, a diverse group with phytopathogenic members capable of genetically transforming plants. To inform on the ecology and evolution of agrobacteria, we revealed processes that diversify their effector gene collections. From genome sequences of diverse strains, we identified T6SS loci, functionally validated associated effector genes for toxicity, and predicted genes homologous to those that encode proteins known to interact with effectors. The gene loci were analyzed in a phylogenetic framework, and results show that strains of some species-level groups have different patterns of T6SS expression and are enriched in specific sets of T6SS loci. Findings also demonstrate that the modularity of T6SS loci and their associated genes engenders dynamicity, promoting reshuffling of entire loci, fragments therein, and domains to swap toxic effector genes across species. However, diversification is constrained by the need to maintain specific combinations of gene subtypes, congruent with observations that certain genes function together to regulate T6SS loading and activation. Data are consistent with a scenario where species can acquire unique T6SS loci that are then reshuffled across the genus in a restricted manner to generate new combinations of effector genes. IMPORTANCE The T6SS is used by several taxa of Gram-negative bacteria to secrete toxic effector proteins to attack others. Diversification of effector collections shapes bacterial interactions and impacts the health of hosts and ecosystems in which bacteria reside. We uncovered the diversity of T6SS loci across a genus of plant-associated bacteria and show that diversification is driven by the acquisition of new loci and reshuffling among species. However, linkages between specific subtypes of genes need to be maintained to ensure that proteins whose interactions are necessary to activate the T6SS remain together. Results reveal how organization of gene loci and domain structure of genes provides flexibility to diversify under the constraints imposed by the system. Findings inform on the evolution of a mechanism that influences bacterial communities.

Dataset Information

Trade-offs constrain adaptive pathways to the type VI secretion system survival.

Publications

Trade-offs constrain adaptive pathways to the type VI secretion system survival.

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