Quorum‐sensing autoinducer molecules produced by members of a multispecies biofilm promote horizontal gene transfer to Vibrio cholerae
TL;DR: It is demonstrated that comEA transcription and the horizontal acquisition of DNA by V. cholerae are induced in response to purified CAI-1 and AI-2, and also by autoinducers derived from other Vibrios co-cultured with V. Cholerae within a mixed-species biofilm, suggesting that autoinducer communication within a consortium may promote DNA exchange among VibRIos.
Abstract: Vibrio cholerae, the causative agent of cholera and a natural inhabitant of aquatic environments, regulates numerous behaviors using a quorum-sensing (QS) system conserved among many members of the marine genus Vibrio. The Vibrio QS response is mediated by two extracellular autoinducer (AI) molecules: CAI-I, which is produced only by Vibrios, and AI-2, which is produced by many bacteria. In marine biofilms on chitinous surfaces, QS-proficient V. cholerae become naturally competent to take up extracellular DNA. Because the direct role of AIs in this environmental behavior had not been determined, we sought to define the contribution of CAI-1 and AI-2 in controlling transcription of the competence gene, comEA, and in DNA uptake. In this study we demonstrated that comEA transcription and the horizontal acquisition of DNA by V. cholerae are induced in response to purified CAI-1 and AI-2, and also by autoinducers derived from other Vibrios co-cultured with V. cholerae within a mixed-species biofilm. These results suggest that autoinducer communication within a consortium may promote DNA exchange among Vibrios, perhaps contributing to the evolution of these bacterial pathogens.
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TL;DR: Recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed and questions are posed for targeted investigation of surface-specific community-level microbial features to advance understanding ofsurface-associated microbial community ecology and the biogeochemical functions of these communities.
Abstract: SUMMARY Biotic and abiotic surfaces in marine waters are rapidly colonized by microorganisms. Surface colonization and subsequent biofilm formation and development provide numerous advantages to these organisms and support critical ecological and biogeochemical functions in the changing marine environment. Microbial surface association also contributes to deleterious effects such as biofouling, biocorrosion, and the persistence and transmission of harmful or pathogenic microorganisms and their genetic determinants. The processes and mechanisms of colonization as well as key players among the surface-associated microbiota have been studied for several decades. Accumulating evidence indicates that specific cell-surface, cell-cell, and interpopulation interactions shape the composition, structure, spatiotemporal dynamics, and functions of surface-associated microbial communities. Several key microbial processes and mechanisms, including (i) surface, population, and community sensing and signaling, (ii) intraspecies and interspecies communication and interaction, and (iii) the regulatory balance between cooperation and competition, have been identified as critical for the microbial surface association lifestyle. In this review, recent progress in the study of marine microbial surface colonization and biofilm development is synthesized and discussed. Major gaps in our knowledge remain. We pose questions for targeted investigation of surface-specific community-level microbial features, answers to which would advance our understanding of surface-associated microbial community ecology and the biogeochemical functions of these communities at levels from molecular mechanistic details through systems biological integration.
696 citations
Additional excerpts
...cholerae in multispecies biofilms (558)....
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TL;DR: It is argued that the lack of environment-facing mitigation actions included in existing AMR action plans is likely a function of the authors' poor fundamental understanding of many of the key issues and the science to inform policy is lacking and this needs to be addressed.
Abstract: The environment is increasingly being recognised for the role it might play in the global spread of clinically-relevant antibiotic resistance. Environmental regulators monitor and control many of the pathways responsible for the release of resistance-driving chemicals into the environment (e.g., antimicrobials, metals, biocides). Hence, environmental regulators should be contributing significantly to the development of global and national antimicrobial resistance (AMR) action plans. It is argued that the lack of environment-facing mitigation actions included in existing AMR action plans is likely a function of our poor fundamental understanding of many of the key issues. Here, we aim to present the problem with AMR in the environment through the lens of an environmental regulator, using the Environment Agency (England’s regulator) as an example from which parallels can be drawn globally. The issues that are pertinent to environmental regulators are drawn out to answer: What are the drivers and pathways of AMR? How do these relate to the normal work, powers and duties of environmental regulators? What are the knowledge gaps that hinder the delivery of environmental protection from AMR? We offer several thought experiments for how different mitigation strategies might proceed. We conclude that: 1) AMR Action Plans do not tackle all the potentially relevant pathways and drivers of AMR in the environment; and 2) AMR Action Plans are deficient, in part, because the science to inform policy is lacking and this needs to be addressed.
525 citations
Cites background from "Quorum‐sensing autoinducer molecule..."
...Many additional drivers (e.g., chemical and environmental) of HGT have been identified (Hastings et al., 2004; Antonova and Hammer, 2011), including abiotic sources (Warnes et al., 2012; Kotnik, 2013)....
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TL;DR: A comprehensive review of the discovery and early characterization of AI-2, current developments in signal detection, transduction and regulation, and the major studies investigating the phenotypes regulated by this molecule is presented.
Abstract: Success in nature depends upon an ability to perceive and adapt to the surrounding environment. Bacteria are not an exception; they recognize and constantly adjust to changing situations by sensing environmental and self-produced signals, altering gene expression accordingly. Autoinducer-2 (AI-2) is a signal molecule produced by LuxS, an enzyme found in many bacterial species and thus proposed to enable interspecies communication. Two classes of AI-2 receptors and many layers and interactions involved in downstream signalling have been identified so far. Although AI-2 has been implicated in the regulation of numerous niche-specific behaviours across the bacterial kingdom, interpretation of these results is complicated by the dual role of LuxS in signalling and the activated methyl cycle, a crucial central metabolic pathway. In this article, we present a comprehensive review of the discovery and early characterization of AI-2, current developments in signal detection, transduction and regulation, and the major studies investigating the phenotypes regulated by this molecule. The development of novel tools should help to resolve many of the remaining questions in the field; we highlight how these advances might be exploited in AI-2 quorum quenching, treatment of diseases, and the manipulation of beneficial behaviours caused by polyspecies communities.
433 citations
TL;DR: The recent focus on complex bacterial communities has led to the recognition of interactions across species boundaries, particularly pronounced in multispecies biofilms, where synergistic interactions impact the bacterial distribution and overall biomass produced.
400 citations
TL;DR: A critical review of QS and how it relates to biofilms in engineered water and wastewater treatment systems and identifies needs for future research is provided.
Abstract: Bacteria have their own form of “twitter” communication, described as quorum sensing (QS), where bacteria emit and sense chemical signal molecules as a means to gauge population density and control gene expression. Many QS-controlled genes relate to biofilm formation and function and may be important for some water and wastewater treatment biofilms. There is a need to better understand bacterial QS, the bacteria biofilm aspects influenced by QS in engineered reactors, and to assess how designs and operations might be improved by taking this signaling into account. This paper provides a critical review of QS and how it relates to biofilms in engineered water and wastewater treatment systems and identifies needs for future research.
256 citations
References
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TL;DR: This study is the first to report a higher frequency of natural mutators among Vibrio environmental strains and to provide evidence that inactivation of MMR increases the diversity of V. parahaemolyticus.
Abstract: Inactivation of mismatch repair (MMR) has been shown to increase the accumulation of spontaneous mutations and frequency of recombination for diverse pathogenic bacteria Currently, little is known regarding the role of mutator phenotypes for the diversification of natural populations of opportunistic human pathogens in marine environments In this study, a higher frequency of mutators was detected among V parahaemolyticus strains obtained from environmental sources compared with clinical sources Inactivation of the MMR gene mutS caused increased antibiotic resistance and phase variation resulting in translucent colony morphologies Increased nucleotide diversity in mutS and rpoB alleles from mutator compared with wild-type strains indicated a significant contribution of the mutator phenotype to the evolution of select genes The results of this study indicate that the inactivation of MMR in V parahaemolyticus leads to increased genetic and phenotypic diversity This study is the first to report a higher frequency of natural mutators among Vibrio environmental strains and to provide evidence that inactivation of MMR increases the diversity of V parahaemolyticus
25 citations
"Quorum‐sensing autoinducer molecule..." refers background in this paper
...…indicate that naturally occurring MMR-deficient environmental ‘mutator’ strains of V. parahaemolyticus have increased genetic and phenotypic diversity relative to clinical isolates, suggesting that such mutator strains are also ‘promiscuous’ for interspecies DNA uptake (Hazen et al., 2009)....
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01 Jan 2008
TL;DR: The authors have restricted the discussion to AI-2 and how that pertains to Vibrio QS, and revealed that in V. harveyi the quorum-regulatory RNAs (Qrr) sRNAs act additively to control luxR mRNA levels.
Abstract: The marine animal pathogen Vibrio harveyi and the human pathogen Vibrio cholerae are aquatic bacteria that engage in a process of cell-cell communication called quorum sensing (QS). Autoinducer (AI)-2 is derived from S-adenosylmethionine in three enzymatic steps. First, S-adenosylmethionine serves as a methyl donor for many biochemical processes, and these methyltransferase-dependent reactions yield S-adenosylhomocysteine. Second, S-adenosylhomocysteine is metabolized to adenine and S-ribosylhomocysteine by the enzyme Pfs, and third, S-ribosylhomocysteine is the substrate for the LuxS enzyme. In mixed species consortia, other microbes also have the potential to alter AI-2 levels, and other classes of AIs are clearly manipulated, but the authors have restricted the discussion to AI-2 and how that pertains to Vibrio QS. Appropriate and distinct responses to potentially different communities are possible because of signal integration in the Vibrio circuits. Channel proteins LsrC and LsrD mediate the delivery of the ligand across the membrane. LsrA is an ATPase that supplies the energy required for transport. Rapid Lsr-dependent transport of R-THMF into the cell occurs at high cell densities. Recent studies in V. harveyi show that it possesses five qrr genes, like its closest Vibrio relatives. Examination of their functions reveals that, in stark contrast to V. cholerae, in V. harveyi the quorum-regulatory RNAs (Qrr) sRNAs act additively to control luxR mRNA levels.
7 citations
"Quorum‐sensing autoinducer molecule..." refers background in this paper
...In this study we demonstrated that comEA transcription and the horizontal acquisition of DNA by V. cholerae are induced in response to purified CAI-1 and AI-2, and also by autoinducers derived from other Vibrios co-cultured with V. cholerae within a mixed-species biofilm....
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...4), which encodes a V. cholerae QS pathway (Hammer & Bassler, 2008)....
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...As with V. cholerae, the maximal transformation frequency occurred with the WT V. harveyi strain, which produces both CAI-1 and AI-2....
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...Recognizing that many Vibrios possess V. cholerae-like QS circuits and produce CAI-1 and AI-2, we examined the relationship between autoinducers production and DNA uptake....
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...Purified autoinducer molecules activate the comEA gene and DNA uptake by V. cholerae To test directly the role of autoinducers in comEA transcription and DNA uptake, purified CAI-1 and AI-2 where applied to the V. cholerae autoinducer-deficient DcqsA DluxS mutant under the conditions described above....
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