Inter-kingdom signaling between gut microbiota and their host

Li, Qing; Ren, Yixing; Fu, Xiangsheng

doi:10.1007/s00018-019-03076-7

Cited by 38 publications

(19 citation statements)

References 59 publications

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“…In recent decades, host hormones and QS of bacteria were found to be effective regulators of crosstalk between bacteria and their host [16,17]. The inter-kingdom signalling between them provides a new way to understand microbial infections and host immunity.…”

Section: Discussionmentioning

confidence: 99%

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Zinc is an important inter-kingdom signal between the host and microbe

Xia

Lian

et al. 2021

Vet Res

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Zinc (Zn) is an essential trace element in living organisms and plays a vital role in the regulation of both microbial virulence and host immune responses. A growing number of studies have shown that zinc deficiency or the internal Zn concentration does not meet the needs of animals and microbes, leading to an imbalance in zinc homeostasis and intracellular signalling pathway dysregulation. Competition for zinc ions (Zn2+) between microbes and the host exists in the use of Zn2+ to maintain cell structure and physiological functions. It also affects the interplay between microbial virulence factors and their specific receptors in the host. This review will focus on the role of Zn in the crosstalk between the host and microbe, especially for changes in microbial pathogenesis and nociceptive neuron-immune interactions, as it may lead to new ways to prevent or treat microbial infections.

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Section: Discussionmentioning

confidence: 99%

“…Thus, zinc is likely to be a potential inter-kingdom signal between the host and microbes. In this review, we describe recent advances in understanding the role of zinc, similar to host hormones and quorum sensing (QS) of bacteria [16,17], in modulating the communication between pathogenic microbes and their hosts.…”

Section: Table Of Contentsmentioning

confidence: 99%

Zinc is an important inter-kingdom signal between the host and microbe

Xia

Lian

et al. 2021

Vet Res

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“…For example, quorum-sensing pathways drive behavior across domains in both mutualistic and parasitic relationships. Examples include communication between the gut and the microbiome (55), competition between C. albicans and P. aeruginosa during infection of the lung (56), and the ability of Legionella pneumophila to alter eukaryotic host cell migration (57). Beyond bacteria and eukaryotes, recent work demonstrates that quorum-sensing-mediated cross-communication occurs between bacteria and phages (58–60).…”

Section: Discussionmentioning

confidence: 99%

Saccharomyces cerevisiaeRequiresCFF1to Produce 4-hydroxy-5-methylfuran-3(2H)-one, a Mimic of the Bacterial Quorum-Sensing Autoinducer AI-2

Valastyan

Kraml

Pelczer

et al. 2020

Preprint

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Quorum sensing is a process of cell-to-cell communication that bacteria use to orchestrate collective behaviors. Quorum sensing depends on the production, release, and detection of extracellular signal molecules called autoinducers (AIs) that accumulate with increasing cell density. While most AIs are species-specific, the AI called AI-2 is produced and detected by diverse bacterial species and it mediates inter-species communication. We recently reported that mammalian cells produce an AI-2 mimic that can be detected by bacteria through the AI-2 receptor, LuxP, potentially expanding the role of the AI-2 system to inter-domain communication. Here, we describe a second molecule capable of inter-domain signaling through LuxP, 4-hydroxy-5-methylfuran-3(2H)-one (MHF) that is produced by the yeast Saccharomyces cerevisiae. Screening the S. cerevisiae deletion collection revealed Cff1p, a protein with no known role, to be required for MHF production. Cff1p is proposed to be an enzyme, possibly an epimerase or isomerase, and substitution at the putative catalytic residue eliminated MHF production in S. cerevisiae. Sequence analysis uncovered Cff1p homologs in many species, primarily bacterial and fungal, but also viral, archaeal, and higher eukaryotic. Cff1p homologs from organisms from all domains can complement a S. cerevisiae cff1Δ mutant and restore MHF production. In all test cases, the identified catalytic residue is conserved and required for MHF to be produced. These findings increase the scope of possibilities for inter-domain interactions via AI-2 and AI-2 mimics, highlighting the breadth of molecules and organisms that could participate in quorum sensing.ImportanceQuorum sensing is a cell-to-cell communication process that bacteria use to monitor local population density. Quorum sensing relies on extracellular signal molecules called autoinducers (AIs). One AI, called AI-2, is broadly made by bacteria and used for inter-species communication. Here, we describe a eukaryotic AI-2 mimic, 5-methylfuran-3(2H)-one, (MHF), that is made by the yeast Saccharomyces cerevisiae, and we identify the Cff1p protein as essential for MHF production. Hundreds of viral, archaeal, bacterial, and eukaryotic organisms possess Cff1p homologs. This finding, combined with our results showing that homologs from all domains can replace S. cerevisiae Cff1p, suggests that like AI-2, MHF is widely produced. Our results expand the breadth of organisms that may participate in quorum-sensing-mediated interactions.

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“…QSMs are also detected by immune cells and regulate the activity of both innate and adaptive immunity. For instance, bacterial autoinducers (Ais) elicit proinflammatory effects and modulate the activities of gut-associated T lymphocytes, macrophages, DCs, and neutrophils [ 220 ]. Moreover, Mast Cell activation through the mast-cell-specific GPCR, MRGPRX2, which are Gram-positive QSMs receptors [ 221 ] leads to degranulation and release of ROS, TNF-α, and Prostaglandin D2, thereby triggering a local inflammatory response.…”

Section: Microbiota-derived Metabolites That Modulate Host Immunity In the Gutmentioning

confidence: 99%

What We Know So Far about the Metabolite-Mediated Microbiota-Intestinal Immunity Dialogue and How to Hear the Sound of This Crosstalk

et al. 2021

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Trillions of microorganisms, termed the “microbiota”, reside in the mammalian gastrointestinal tract, and collectively participate in regulating the host phenotype. It is now clear that the gut microbiota, metabolites, and intestinal immune function are correlated, and that alterations of the complex and dynamic host-microbiota interactions can have deep consequences for host health. However, the mechanisms by which the immune system regulates the microbiota and by which the microbiota shapes host immunity are still not fully understood. This article discusses the contribution of metabolites in the crosstalk between gut microbiota and immune cells. The identification of key metabolites having a causal effect on immune responses and of the mechanisms involved can contribute to a deeper insight into host-microorganism relationships. This will allow a better understanding of the correlation between dysbiosis, microbial-based dysmetabolism, and pathogenesis, thus creating opportunities to develop microbiota-based therapeutics to improve human health. In particular, we systematically review the role of soluble and membrane-bound microbial metabolites in modulating host immunity in the gut, and of immune cells-derived metabolites affecting the microbiota, while discussing evidence of the bidirectional impact of this crosstalk. Furthermore, we discuss the potential strategies to hear the sound of such metabolite-mediated crosstalk.

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Inter-kingdom signaling between gut microbiota and their host

Cited by 38 publications

References 59 publications

Zinc is an important inter-kingdom signal between the host and microbe

Zinc is an important inter-kingdom signal between the host and microbe

Saccharomyces cerevisiaeRequiresCFF1to Produce 4-hydroxy-5-methylfuran-3(2H)-one, a Mimic of the Bacterial Quorum-Sensing Autoinducer AI-2

What We Know So Far about the Metabolite-Mediated Microbiota-Intestinal Immunity Dialogue and How to Hear the Sound of This Crosstalk

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