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1. LuxT Is a Global Regulator of Low-Cell-Density Behaviors, Including Type III Secretion, Siderophore Production, and Aerolysin Production, in Vibrio harveyi

   https://doi.org/10.1128/mbio.03621-21  

   Eickhoff, Michaela J. ; Fei, Chenyi ; Cong, Jian-Ping ; Bassler, Bonnie L. ( February 2022 , mBio)

   Storz, Gisela (Ed.)

   ABSTRACT Quorum sensing (QS) is a chemical communication process in which bacteria produce, release, and detect extracellular signaling molecules called autoinducers. Via combined transcriptional and posttranscriptional regulatory mechanisms, QS allows bacteria to collectively alter gene expression on a population-wide scale. Recently, the TetR family transcriptional regulator LuxT was shown to control Vibrio harveyi qrr 1, encoding the Qrr1 small RNA that functions at the core of the QS regulatory cascade. Here, we use RNA sequencing to reveal that, beyond the control of qrr 1, LuxT is a global regulator of 414 V. harveyi genes, including those involved in type III secretion, siderophore production, and aerolysin toxin biosynthesis. Importantly, LuxT directly represses swrZ , encoding a GntR family transcriptional regulator, and LuxT control of type III secretion, siderophore, and aerolysin genes occurs by two mechanisms, one that is SwrZ dependent and one that is SwrZ independent. All of these target genes specify QS-controlled behaviors that are enacted when V. harveyi is at low cell density. Thus, LuxT and SwrZ function in parallel with QS to drive particular low-cell-density behaviors. Phylogenetic analyses reveal that luxT is highly conserved among Vibrionaceae , but swrZ is less well conserved. In a test case, we find that in Aliivibrio fischeri , LuxT also represses swrZ . SwrZ is a repressor of A. fischeri siderophore production genes. Thus, LuxT repression of swrZ drives the activation of A. fischeri siderophore gene expression. Our results indicate that LuxT is a major regulator among Vibrionaceae , and in the species that also possess swrZ , LuxT functions with SwrZ to control gene expression. IMPORTANCE Bacteria precisely tune gene expression patterns to successfully react to changes that occur in the environment. Defining the mechanisms that enable bacteria to thrive in diverse and fluctuating habitats, including in host organisms, is crucial for a deep understanding of the microbial world and also for the development of effective applications to promote or combat particular bacteria. In this study, we show that a regulator called LuxT controls over 400 genes in the marine bacterium Vibrio harveyi and that LuxT is highly conserved among Vibrionaceae species, ubiquitous marine bacteria that often cause disease. We characterize the mechanisms by which LuxT controls genes involved in virulence and nutrient acquisition. We show that LuxT functions in parallel with a set of regulators of the bacterial cell-to-cell communication process called quorum sensing to promote V. harveyi behaviors at low cell density. 

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2. Persistent symbiont colonization leads to a maturation of hemocyte response in the Euprymna scolopes / Vibrio fischeri symbiosis

   https://doi.org/10.1002/mbo3.858  

   Rader, Bethany ; McAnulty, Sarah J. ; Nyholm, Spencer V. ( June 2019 , MicrobiologyOpen)

   The binary association between the squid,Euprymna scolopes, and its symbiont,Vibrio fischeri, serves as a model system to study interactions between beneficial bacteria and the innate immune system. Previous research demonstrated that binding of the squid's immune cells, hemocytes, toV. fischeriis altered if the symbiont is removed from the light organ, suggesting that host colonization alters hemocyte recognition ofV. fischeri. To investigate the influence of symbiosis on immune maturation during development, we characterized hemocyte binding and phagocytosis ofV. fischeriand nonsymbioticVibrio harveyifrom symbiotic (sym) and aposymbiotic (apo) juveniles, and wild‐caught and laboratory‐raised sym and apo adults. Our results demonstrate that while light organ colonization byV. fischeridid not alter juvenile hemocyte response, these cells bound a similar number ofV. fischeriandV. harveyiyet phagocytosed onlyV. harveyi. Our results also indicate that long‐term colonization altered the adult hemocyte response toV. fischeribut notV. harveyi. All hemocytes from adult squid, regardless of apo or sym state, both bound and phagocytosed a similar number ofV. harveyiwhile hemocytes from both wild‐caught and sym‐raised adults bound significantly fewerV. fischeri, although moreV. fischeriwere phagocytosed by hemocytes from wild‐caught animals. In contrast, hemocytes from apo‐raised squid bound similar numbers of bothV. fischeriandV. harveyi, although moreV. harveyicells were engulfed, suggesting that blood cells from apo‐raised adults behaved similarly to juvenile hosts. Taken together, these data suggest that persistent colonization by the light organ symbiont is required for hemocytes to differentially bind and phagocytoseV. fischeri. The cellular immune system ofE. scolopeslikely possesses multiple mechanisms at different developmental stages to promote a specific and life‐long interaction with the symbiont.

    

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3. Virulence as a Side Effect of Interspecies Interaction in Vibrio Coral Pathogens

   https://doi.org/10.1128/mBio.00201-20  

   Rubio-Portillo, Esther ; Martin-Cuadrado, Ana B. ; Caraballo-Rodríguez, Andrés M. ; Rohwer, Forest ; Dorrestein, Pieter C. ; Antón, Josefa ( August 2020 , mBio)

   Dubilier, Nicole (Ed.)

   ABSTRACT The increase in prevalence and severity of coral disease outbreaks produced by Vibrio pathogens, and related to global warming, has seriously impacted reef-building corals throughout the oceans. The coral Oculina patagonica has been used as a model system to study coral bleaching produced by Vibrio infection. Previous data demonstrated that when two coral pathogens ( Vibrio coralliilyticus and Vibrio mediterranei ) simultaneously infected the coral O. patagonica , their pathogenicity was greater than when each bacterium was infected separately. Here, to understand the mechanisms underlying this synergistic effect, transcriptomic analyses of monocultures and cocultures as well as experimental infection experiments were performed. Our results revealed that the interaction between the two vibrios under culture conditions overexpressed virulence factor genes (e.g., those encoding siderophores, the type VI secretion system, and toxins, among others). Moreover, under these conditions, vibrios were also more likely to form biofilms or become motile through induction of lateral flagella. All these changes that occur as a physiological response to the presence of a competing species could favor the colonization of the host when they are present in a mixed population. Additionally, during coral experimental infections, we showed that exposure of corals to molecules released during V. coralliilyticus and V. mediterranei coculture induced changes in the coral microbiome that favored damage to coral tissue and increased the production of lyso-platelet activating factor. Therefore, we propose that competition sensing, defined as the physiological response to detection of harm or to the presence of a competing Vibrio species, enhances the ability of Vibrio coral pathogens to invade their host and cause tissue necrosis. IMPORTANCE Vibrio coralliilyticus and Vibrio mediterranei are important coral pathogens capable of inducing serious coral damage, which increases severely when they infect the host simultaneously. This has consequences related to the dispersion of these pathogens among different locations that could enhance deleterious effects on coral reefs. However, the mechanisms underlying this synergistic interaction are unknown. The work described here provides a new perspective on the complex interactions among these two Vibrio coral pathogens, suggesting that coral infection could be a collateral effect of interspecific competition. Major implications of this work are that (i) Vibrio virulence mechanisms are activated in the absence of the host as a response to interspecific competition and (ii) release of molecules by Vibrio coral pathogens produces changes in the coral microbiome that favor the pathogenic potential of the entire Vibrio community. Thus, our results highlight that social cues and competition sensing are crucial determinants of development of coral diseases. 

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4. Nickel exposure reduces enterobactin production in Escherichia coli

   https://doi.org/10.1002/mbo3.691  

   Washington – Hughes, Clorissa L. ; Ford, Geoffrey T. ; Jones, Alsten D. ; McRae, Kimberly ; Outten, F. Wayne ( July 2018 , MicrobiologyOpen)

   Escherichia coliis a well‐studied bacterium that can be found in many niches, such as industrial wastewater, where the concentration of nickel can rise to low‐millimolar levels. Recent studies show that nickel exposure can repress pyochelin or induce pyoverdine siderophore production inPseudomonas aueroginosa. Understanding the molecular cross‐talk between siderophore production, metal homeostasis, and metal toxicity in microorganisms is critical for designing bioremediation strategies for metal‐contaminated sites. Here, we show that high‐nickel exposure prolongs lag phase duration as a result of low‐intracellular iron levels inE. coli. AlthoughE. colicells respond to low‐intracellular iron during nickel stress by maintaining high expression of iron uptake systems such asfepA, the demand for iron is not met due to a lack of siderophores in the extracellular medium during nickel stress. Taken together, these results indicate that nickel inhibits iron accumulation inE. coliby reducing the presence of enterobactin in the extracellular medium.

    

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5. Petrobactin, a siderophore produced by Alteromonas , mediates community iron acquisition in the global ocean

   https://doi.org/10.1038/s41396-021-01065-y  

   Manck, Lauren E. ; Park, Jiwoon ; Tully, Benjamin J. ; Poire, Alfonso M. ; Bundy, Randelle M. ; Dupont, Christopher L. ; Barbeau, Katherine A. ( August 2021 , The ISME Journal)

   It is now widely accepted that siderophores play a role in marine iron biogeochemical cycling. However, the mechanisms by which siderophores affect the availability of iron from specific sources and the resulting significance of these processes on iron biogeochemical cycling as a whole have remained largely untested. In this study, we develop a model system for testing the effects of siderophore production on iron bioavailability using the marine copiotroph Alteromonas macleodii ATCC 27126. Through the generation of the knockout cell line ΔasbB::kmr, which lacks siderophore biosynthetic capabilities, we demonstrate that the production of the siderophore petrobactin enables the acquisition of iron from mineral sources and weaker iron-ligand complexes. Notably, the utilization of lithogenic iron, such as that from atmospheric dust, indicates a significant role for siderophores in the incorporation of new iron into marine systems. We have also detected petrobactin, a photoreactive siderophore, directly from seawater in the mid-latitudes of the North Pacific and have identified the biosynthetic pathway for petrobactin in bacterial metagenome-assembled genomes widely distributed across the global ocean. Together, these results improve our mechanistic understanding of the role of siderophore production in iron biogeochemical cycling in the marine environment wherein iron speciation, bioavailability, and residence time can be directly influenced by microbial activities.

    

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