Dataset Information

Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts.

ABSTRACT: Bacterial communities colonize epithelial surfaces of most animals. Several factors, including the innate immune system, mucus composition, and diet, have been identified as determinants of host-associated bacterial communities. Here we show that the early branching metazoan Hydra is able to modify bacterial quorum-sensing signals. We identified a eukaryotic mechanism that enables Hydra to specifically modify long-chain 3-oxo-homoserine lactones into their 3-hydroxy-HSL counterparts. Expression data revealed that Hydra's main bacterial colonizer, Curvibacter sp., responds differentially to N-(3-hydroxydodecanoyl)-l-homoserine lactone (3OHC12-HSL) and N-(3-oxododecanoyl)-l-homoserine lactone (3OC12-HSL). Investigating the impacts of the different N-acyl-HSLs on host colonization elucidated that 3OHC12-HSL allows and 3OC12-HSL represses host colonization of Curvibacter sp. These results show that an animal manipulates bacterial quorum-sensing signals and that this modification leads to a phenotypic switch in the bacterial colonizers. This mechanism may enable the host to manipulate the gene expression and thereby the behavior of its bacterial colonizers.

SUBMITTER: Pietschke C

PROVIDER: S-EPMC5635886 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts.

Pietschke Cleo C Treitz Christian C Forêt Sylvain S Schultze Annika A Künzel Sven S Tholey Andreas A Bosch Thomas C G TCG Fraune Sebastian S

Proceedings of the National Academy of Sciences of the United States of America 20170918 40

Bacterial communities colonize epithelial surfaces of most animals. Several factors, including the innate immune system, mucus composition, and diet, have been identified as determinants of host-associated bacterial communities. Here we show that the early branching metazoan <i>Hydra</i> is able to modify bacterial quorum-sensing signals. We identified a eukaryotic mechanism that enables <i>Hydra</i> to specifically modify long-chain 3-oxo-homoserine lactones into their 3-hydroxy-HSL counterpart ...[more]

PMID: 28923926

Similar Datasets

Project description:Interactions between phytoplankton and heterotrophic bacteria fundamentally shape marine ecosystems by controlling primary production, structuring marine food webs, mediating carbon export, and influencing global climate. Phytoplankton-bacterium interactions are facilitated by secreted compounds; however, linking these chemical signals, their mechanisms of action, and their resultant ecological consequences remains a fundamental challenge. The bacterial quorum-sensing signal 2-heptyl-4-quinolone (HHQ) induces immediate, yet reversible, cellular stasis (no cell division or mortality) in the coccolithophore Emiliania huxleyi; however, the mechanism responsible remains unknown. Using transcriptomic and proteomic approaches in combination with diagnostic biochemical and fluorescent cell-based assays, we show that HHQ exposure leads to prolonged S-phase arrest in phytoplankton coincident with the accumulation of DNA damage and a lack of repair despite the induction of the DNA damage response (DDR). While this effect is reversible, HHQ-exposed phytoplankton were also protected from viral mortality, ascribing a new role of quorum-sensing signals in regulating multitrophic interactions. Furthermore, our data demonstrate that in situ measurements of HHQ coincide with areas of enhanced micro- and nanoplankton biomass. Our results suggest bacterial communication signals as emerging players that may be one of the contributing factors that help structure complex microbial communities throughout the ocean.IMPORTANCE Bacteria and phytoplankton form close associations in the ocean that are driven by the exchange of chemical compounds. The bacterial signal 2-heptyl-4-quinolone (HHQ) slows phytoplankton growth; however, the mechanism responsible remains unknown. Here, we show that HHQ exposure leads to the accumulation of DNA damage in phytoplankton and prevents its repair. While this effect is reversible, HHQ-exposed phytoplankton are also relieved of viral mortality, elevating the ecological consequences of this complex interaction. Further results indicate that HHQ may target phytoplankton proteins involved in nucleotide biosynthesis and DNA repair, both of which are crucial targets for viral success. Our results support microbial cues as emerging players in marine ecosystems, providing a new mechanistic framework for how bacterial communication signals mediate interspecies and interkingdom behaviors.

Project description:Bacterial viruses, or bacteriophages, are highly abundant in the biosphere and have a major impact on microbial populations. Many examples of phage interactions with their hosts, including establishment of dormant lysogenic and active lytic states, have been characterized at the level of the individual cell. However, much less is known about the dependence of these interactions on host metabolism and signal exchange within bacterial communities. In this report, we describe a lysogenic state of the enterobacterial phage T1, previously known as a classical lytic phage, and characterize the underlying regulatory circuitry. We show that the transition from lysogeny to lysis depends on bacterial population density, perceived via interspecies autoinducer 2. Lysis is further controlled by the metabolic state of the cell, mediated by the cyclic-3',5'-AMP (cAMP) receptor protein (CRP) of the host. We hypothesize that such combinations of cell density and metabolic sensing may be common in phage-host interactions.IMPORTANCE The dynamics of microbial communities are heavily shaped by bacterium-bacteriophage interactions. But despite the apparent importance of bacteriophages, our understanding of the mechanisms controlling phage dynamics in bacterial populations, and particularly of the differences between the decisions that are made in the dormant lysogenic and active lytic states, remains limited. In this report, we show that enterobacterial phage T1, previously described as a lytic phage, is able to undergo lysogeny. We further demonstrate that the lysogeny-to-lysis decision occurs in response to changes in the density of the bacterial population, mediated by interspecies quorum-sensing signal AI-2, and in the metabolic state of the cell, mediated by cAMP receptor protein. We hypothesize that this strategy enables the phage to maximize its chances of self-amplification and spreading in bacterial population upon induction of the lytic cycle and that it might be common in phage-host interactions.

Dataset Information

Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts.

Publications

Host modification of a bacterial quorum-sensing signal induces a phenotypic switch in bacterial symbionts.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets