Quorum Quenching of Nitrobacter winogradskyi Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification

Mellbye, Brett L.; Giguere, Andrew T.; Bottomley, Peter J.; Sayavedra-Soto, Luis A.

doi:10.1128/mbio.01753-16

Cited by 53 publications

(32 citation statements)

References 56 publications

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“…Toyofuku et al (26) reported that P. aeruginosa quorum-sensing regulators LasR and RhlR could inhibit denitrification. Similarly, Nitrobacter winogradskyi significantly increased the expression of nirK and nirK cluster genes (genes involved in denitrification) after quorum quenching (27). In our study, the addition of NaNO 3 or NaNO 2 changed the rate of denitrification (Fig.…”

Section: Discussionsupporting

confidence: 67%

Nitrogen Source Stabilization of Quorum Sensing in the Pseudomonas aeruginosa Bioaugmentation Strain SD-1

Wang

Lai

Dandekar

et al. 2017

Appl Environ Microbiol

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Pseudomonas aeruginosa SD-1 is efficient at degrading aromatic compounds and can therefore contribute to the bioremediation of wastewater. P. aeruginosa uses quorum sensing (QS) to regulate the production of numerous secreted "public goods." In wastewater bioaugmentation applications, there are myriad nitrogen sources, and we queried whether various nitrogen sources impact the stabilities of both QS and the bacterial populations. In a laboratory strain of P. aeruginosa, PAO1, the absence of a nitrogen source has been shown to destabilize these populations through the emergence of QS mutant "cheaters." We tested the ability of SD-1 to grow in casein broth, a condition that requires QS for growth, when the nitrogen source with either NH 4 Cl, NaNO 3 , or NaNO 2 or with no added nitrogen source. There was great variability in susceptibility to invasion by QS mutant cheaters and, by extension, the stability of the SD-1 population. When grown with NH 4 Cl as an extra nitrogen source, no population collapse was observed; by contrast, twothirds of cultures grown in the presence of NaNO 2 collapsed. In the populations that collapsed, the frequency of social cheaters exceeded 40%. NaNO 3 and NaNO 2 directly favor QS mutants of P. aeruginosa SD-1. Although the mechanism by which these nitrogen sources act is not clear, these data indicate that the metabolism of nitrogen can affect the stability of bacterial populations, an important observation for continuing industrial applications with this species.IMPORTANCE Bioaugmentation as a method to help remediate wastewater pollutant streams holds significant potential to enhance traditional methods of treatment. Addition of microbes that can catabolize organic pollutants can be an effective method to remove several toxic compounds. Such bioaugmented strains of bacteria have been shown to be susceptible to competition from the microbiota that are present in wastewater streams, limiting their potential effectiveness. Here, we show that bioaugmentation strains of bacteria might also be susceptible to invasion by social cheaters and that the nitrogen sources available in the wastewater might influence the ability of cheaters to overtake the bioaugmentation strains. Our results imply that control over the nitrogen sources in a wastewater stream or selective addition of certain nitrogen sources could help stabilize bioaugmentation strains of bacteria.KEYWORDS quorum sensing, social cheating, bioaugmentation, long-term stabilization, inorganic nitrogen B ioaugmentation, the use of selected microbial strains in activated sludge to strengthen their abilities for pollutant removal (1), has significant advantages in the degradation of toxic and hazardous compounds. These advantages include cost and

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Section: Discussionsupporting

confidence: 67%

Nitrogen Source Stabilization of Quorum Sensing in the Pseudomonas aeruginosa Bioaugmentation Strain SD-1

Wang

Lai

Dandekar

et al. 2017

Appl Environ Microbiol

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“…Our current model does not consider acyl-homoserine lactone quorum sensing (QS) regulation of NO production proposed in recent work by Mellbye et al due to insufficient data on the kinetic effects of QS regulation (16). The genome-scale model also does not consider the minute N 2 O production observed by N. winogradskyi , since its genome does not contain any known NOR-encoding gene.…”

Section: Discussionmentioning

confidence: 99%

“…Extracellular NH 2 OH concentration was measured by chemical assay as previously described (58, 59). NO and NO 2 (NO x ) concentrations in the headspace were measured using a portable NO 2 analyzer/NO x converter (LMA-3D and LNC-3D; Unisearch Associates Ltd., Concord, Ontario, Canada), and N 2 O concentration was measured by gas chromatography as previously described (16, 21). …”

Section: Methodsmentioning

confidence: 99%

Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

et al. 2018

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Modern agriculture is sustained by application of inorganic nitrogen (N) fertilizer in the form of ammonium (NH4+). Up to 60% of NH4+-based fertilizer can be lost through leaching of nitrifier-derived nitrate (NO3−), and through the emission of N oxide gases (i.e., nitric oxide [NO], N dioxide [NO2], and nitrous oxide [N2O] gases), the latter being a potent greenhouse gas. Our approach to modeling of nitrification suggests that both biotic and abiotic mechanisms function as important sources and sinks of N oxides during microaerobic conditions and that previous models might have underestimated gross NO production during nitrification.

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“…Using a novel quorum quenching coupled with mRNA sequencing approach, Mellbye et al . () revealed that QS signalling influences production and consumption of NO, NO 2 and N 2 O in a model nitrite oxidizer, Nitrobacter winogradskyi . QS mediated expression of genes can also regulate inter/intra kingdom signalling in microbiome.…”

Section: The Potential Of Emerging Microbiome‐based Technologies For mentioning

confidence: 99%

“…However, this approach may have indirect effects on other Ncycling processes, as these microbes have strong and constant associations and closely interact with each other to produce N 2 O (Butterbach-Bahl et al, 2013). Using a novel quorum quenching coupled with mRNA sequencing approach, Mellbye et al (2016) revealed that QS signalling influences production and consumption of NO, NO 2 and N 2 O in a model nitrite oxidizer, Nitrobacter winogradskyi. QS mediated expression of genes can also regulate inter/intra kingdom signalling in microbiome.…”

Section: Mozzola 2002mentioning

confidence: 99%

Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation

Trivedi

Singh

2017

Environmental Microbiology

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Globally, drylands represent the largest terrestrial biome and are projected to expand by 23% by the end of this century. Drylands are characterized by extremely low levels of water and nutrients and exhibit highly heterogeneous distribution in plants and biocrusts which make microbial processes shaping the dryland functioning rather unique compared with other terrestrial ecosystems. Nitrous oxide (N O) is a powerful greenhouse gas with ozone depletion potential. Despite of the pivotal influences of microbial communities on the production and consumption of N O, we have limited knowledge of the biological pathways and mechanisms underpinning N O emissions from drylands, which are estimated to account for 30% of total gaseous nitrogen emissions on Earth. In this article, we describe the key microbial players and biological pathways regulating dryland N O emissions, and discuss how these processes will respond to emerging global changes such as climate warming, extreme weather events and nitrogen deposition. We also provide a conceptual framework to precisely manipulate the dryland microbiome to mitigate N O emissions in situ using emerging technologies with great specificity and efficacy. These cross-disciplinary efforts will enable the development of novel and environmental-friendly microbiome-based solutions to future mitigation strategies of climate change.

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Quorum Quenching of Nitrobacter winogradskyi Suggests that Quorum Sensing Regulates Fluxes of Nitrogen Oxide(s) during Nitrification

Cited by 53 publications

References 56 publications

Nitrogen Source Stabilization of Quorum Sensing in the Pseudomonas aeruginosa Bioaugmentation Strain SD-1

Nitrogen Source Stabilization of Quorum Sensing in the Pseudomonas aeruginosa Bioaugmentation Strain SD-1

Genome-Scale, Constraint-Based Modeling of Nitrogen Oxide Fluxes during Coculture of Nitrosomonas europaea and Nitrobacter winogradskyi

Microbial nitrous oxide emissions in dryland ecosystems: mechanisms, microbiome and mitigation

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