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: Synthetic (S)-3-hydroxytridecan-4-one functions as effectively as natural CAI-1 in repressing production of the canonical virulence factor TCP (toxin co-regulated pilus) and is suggested to be a new type of bacterial autoinducer.
Abstract: In a process called quorum sensing, certain bacteria can communicate with each other using chemical signalling molecules, allowing them to synchronize gene expression so that they act virtually as multicellular organisms. The cholera pathogen Vibrio cholerae uses quorum sensing to control virulence and to organize the biofilms that contribute to the difficulties of treating the infection. Now the major V. cholerae quorum-sensing signalling molecule, an autoinducer called CAI-1, has been identified and characterized as (S)-3-hydroxytridecan-4-one, a molecule new to biology. Providing CAI-1 to the bacterium terminates the production of factors required for pathogenicity, suggesting a possible new treatment for this major pathogen. Vibrio cholerae, the causative agent of cholera, employs quorum sensing to repress virulence factor expression at high cell density. The nature of one of the major signals is now revealed as (S)-3-hydroxytridecan-4-one constituting a new class of bacterial quorum sensing signalling molecules. Vibrio cholerae, the causative agent of the human disease cholera, uses cell-to-cell communication to control pathogenicity and biofilm formation1,2. This process, known as quorum sensing, relies on the secretion and detection of signalling molecules called autoinducers. At low cell density V. cholerae activates the expression of virulence factors and forms biofilms. At high cell density the accumulation of two quorum-sensing autoinducers represses these traits. These two autoinducers, cholerae autoinducer-1 (CAI-1) and autoinducer-2 (AI-2), function synergistically to control gene regulation, although CAI-1 is the stronger of the two signals. V. cholerae AI-2 is the furanosyl borate diester (2S,4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran borate3. Here we describe the purification of CAI-1 and identify the molecule as (S)-3-hydroxytridecan-4-one, a new type of bacterial autoinducer. We provide a synthetic route to both the R and S isomers of CAI-1 as well as simple homologues, and we evaluate their relative activities. Synthetic (S)-3-hydroxytridecan-4-one functions as effectively as natural CAI-1 in repressing production of the canonical virulence factor TCP (toxin co-regulated pilus). These findings suggest that CAI-1 could be used as a therapy to prevent cholera infection and, furthermore, that strategies to manipulate bacterial quorum sensing hold promise in the clinical arena.
427 citations
"Quorum‐sensing autoinducer molecule..." refers background or methods in this paper
...CAI-1 is the major autoinducer and AI-2 is the minor autoinducer for comEA transcription, as reported for V. cholerae virulence factor production in vivo (Higgins et al., 2007; Duan & March, 2010)....
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...…V. cholerae produces two autoinducers: CAI-I (the product of the CqsA synthase), which is restricted to Vibrios, and AI-2 (the product of the LuxS synthase), an interspecies autoinducer molecule produced by many bacteria (Chen et al., 2002; Xavier & Bassler, 2005; Higgins et al., 2007)....
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...…was incubated as described above, but diluted 1 : 1000 into fresh medium containing purified CAI-1 alone, AI-2 alone, or both autoinducers at a final concentration of 10 mM, and incubated for 8 h. Purified autoinducers were prepared as described (Schauder et al., 2001; Higgins et al., 2007)....
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TL;DR: The results suggest that V. cholerae integrates information about the vicinal bacterial community contained in extracellular QS autoinducers with the intracellular environmental information encoded in c-di-GMP to control biofilm formation.
Abstract: Two chemical signaling systems, quorum sensing (QS) and 3',5'-cyclic diguanylic acid (c-di-GMP), reciprocally control biofilm formation in Vibrio cholerae. QS is the process by which bacteria communicate via the secretion and detection of autoinducers, and in V. cholerae, QS represses biofilm formation. c-di-GMP is an intracellular second messenger that contains information regarding local environmental conditions, and in V. cholerae, c-di-GMP activates biofilm formation. Here we show that HapR, a major regulator of QS, represses biofilm formation in V. cholerae through two distinct mechanisms. HapR controls the transcription of 14 genes encoding a group of proteins that synthesize and degrade c-di-GMP. The net effect of this transcriptional program is a reduction in cellular c-di-GMP levels at high cell density and, consequently, a decrease in biofilm formation. Increasing the c-di-GMP concentration at high cell density to the level present in the low-cell-density QS state restores biofilm formation, showing that c-di-GMP is epistatic to QS in the control of biofilm formation in V. cholerae. In addition, HapR binds to and directly represses the expression of the biofilm transcriptional activator, vpsT. Together, our results suggest that V. cholerae integrates information about the vicinal bacterial community contained in extracellular QS autoinducers with the intracellular environmental information encoded in c-di-GMP to control biofilm formation.
391 citations
TL;DR: Based on the comparative genomics, it is concluded that V. cholerae undergoes extensive genetic recombination via lateral gene transfer, and, therefore, genome assortment, not serogroup, should be used to define pathogenic V.cholerae clones.
Abstract: Vibrio cholerae, the causative agent of cholera, is a bacterium autochthonous to the aquatic environment, and a serious public health threat. V. cholerae serogroup O1 is responsible for the previous two cholera pandemics, in which classical and El Tor biotypes were dominant in the sixth and the current seventh pandemics, respectively. Cholera researchers continually face newly emerging and reemerging pathogenic clones carrying diverse combinations of phenotypic and genotypic properties, which significantly hampered control of the disease. To elucidate evolutionary mechanisms governing genetic diversity of pandemic V. cholerae, we compared the genome sequences of 23 V. cholerae strains isolated from a variety of sources over the past 98 years. The genome-based phylogeny revealed 12 distinct V. cholerae lineages, of which one comprises both O1 classical and El Tor biotypes. All seventh pandemic clones share nearly identical gene content. Using analogy to influenza virology, we define the transition from sixth to seventh pandemic strains as a “shift” between pathogenic clones belonging to the same O1 serogroup, but from significantly different phyletic lineages. In contrast, transition among clones during the present pandemic period is characterized as a “drift” between clones, differentiated mainly by varying composition of laterally transferred genomic islands, resulting in emergence of variants, exemplified by V. cholerae O139 and V. cholerae O1 El Tor hybrid clones. Based on the comparative genomics it is concluded that V. cholerae undergoes extensive genetic recombination via lateral gene transfer, and, therefore, genome assortment, not serogroup, should be used to define pathogenic V. cholerae clones.
364 citations
"Quorum‐sensing autoinducer molecule..." refers background in this paper
...Recent genomic comparison studies of multiple V. cholerae isolates suggest that substantial HGTevents among Vibrio species may account for the presence of large ‘genomic islands’ of transferred DNA (Chun et al., 2009)....
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TL;DR: It is concluded that some condition(s) specific to the internal environment of the light organ is necessary for maximal autoinduction of luminescence in the symbionts of this squid-bacterial association.
Abstract: Bioluminescent marine bacteria of the species Vibrio fischeri are the specific light organ symbionts of the sepiolid squid Euprymna scolopes. Although they share morphological and physiological characteristics with other strains of V. fischeri, when cultured away from the light organ association the E. scolopes symbionts depress their maximal luminescence over 1,000-fold. The primary cause of this reduced luminescence is the underproduction by these bacteria of luciferase autoinducer, a molecule involved in the positive transcriptional regulation of the V. fischeri lux operon. Such an absence of visible light production outside of the symbiotic association has not been previously reported among light organ symbionts of this or any other species of luminous bacteria. Levels of luminescence approaching those of the E. scolopes bacteria in the intact association can be restored by the addition of exogenous autoinducer to bacteria in laboratory culture and are affected by the presence of cyclic AMP. We conclude that some condition(s) specific to the internal environment of the light organ is necessary for maximal autoinduction of luminescence in the symbionts of this squid-bacterial association.
354 citations
01 Jan 1990
TL;DR: In this article, it was shown that when cultured away from the symbiotic association, Euprymna scolopes symbionts depress their maximal luminescence over 1,000 times, and that the primary cause of this reduced luminecence is the underproduction by these bacteria of luciferase autoinducer, a molecule involved in the positive transcriptional regulation of the V. fischeri lux operon.
Abstract: Bioluminescent marine bacteria of the species Vibrio fischeri are the specific light organ symbionts of the sepiolid squid Euprymna scolopes. Although they share morphological and physiological characteristics with other strains of V. fischeri, when cultured away from the light organ association the E. scolopes symbionts depress their maximal luminescence over 1,000-fold. The primary cause of this reduced luminescence is the underproduction by these bacteria of luciferase autoinducer, a molecule involved in the positive transcriptional regulation of the V. fischeri lux operon. Such an absence of visible light production outside of the symbiotic association has not been previously reported among light organ symbionts of this or any other species of luminous bacteria. Levels of luminescence approaching those of the E. scolopes bacteria in the intact association can be restored by the addition of exogenous autoinducer to bacteria in laboratory culture and are affected by the presence of cyclic AMP. We conclude that some condition(s) specific to the internal environment of the light organ is necessary for maximal autoinduction of luminescence in the symbionts of this squid-bacterial association.
352 citations