Commensal bacteria‐immunity crosstalk shapes mucosal homeostasis in teleost fish

Yu, Yongyao; Ding, Li-Guo; Huang, Zhenyu; Xu, Hanqing; Xu, Zhen

doi:10.1111/raq.12570

Cited by 62 publications

(44 citation statements)

References 261 publications

(531 reference statements)

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“…To prevent the microbiota that populates the mucus from gaining access into the mucosal epithelium, sIgA acts through an immune exclusion mechanism in mucosal surfaces by coating different commensal bacteria 40 , 41 . Here we determined that sIgT is the main Ig class that coats the SB microbiota, while a smaller portion of the bacteria was coated by sIgM and sIgD as has been shown also for other trout MALTs 22 , 42 . Interestingly, we found that the SB represented the trout MALT with the lowest concentration of bacteria, a feature that resembles that of the lung.…”

Section: Discussionsupporting

confidence: 67%

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses

Huang

Kong

et al. 2022

Cell Discov

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The air-filled organs (AOs) of vertebrates (lungs and swim bladders) have evolved unique functions (air-breathing or buoyancy control in water) to adapt to different environments. Thus far, immune responses to microbes in AOs have been described exclusively in the lungs of tetrapods. Similar to lungs, swim bladders (SBs) represent a mucosal surface, a feature that leads us to hypothesize a role for SB in immunity. In this study, we demonstrate that secretory IgT (sIgT) is the key SB immunoglobulin (Ig) responding to the viral challenge, and the only Ig involved in viral neutralization in that organ. In support of these findings, we found that the viral load of the SB from fish devoid of sIgT was much higher than that of control fish. Interestingly, similar to the lungs in mammals, the SB represents the mucosal surface in fish with the lowest content of microbiota. Moreover, sIgT is the main Ig class found coating their surface, suggesting a key role of this Ig in the homeostasis of the SB microbiota. In addition to the well-established role of SB in buoyancy control, our findings reveal a previously unrecognized function of teleost SB in adaptive mucosal immune responses upon pathogenic challenge, as well as a previously unidentified role of sIgT in antiviral defense. Overall, our findings indicate that despite the phylogenetic distance and physiological roles of teleost SB and mammalian lungs, they both have evolved analogous mucosal immune responses against microbes which likely originated independently through a process of convergent evolution.

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Section: Discussionsupporting

confidence: 67%

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses

Huang

Kong

et al. 2022

Cell Discov

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“…Synergistic and competitive interactions between host immunity and microbiota emerged in both primitive and modern vertebrates to maintain mucosal tissue surface homeostasis and respond to disease ( 2 , 4 ). The upper respiratory tract of mammals is populated with a vast range of commensals and potentially pathogenic bacteria, which occupy different ecological niches and form a complex microbial community.…”

Section: Discussionmentioning

confidence: 99%

“…The mucosa of vertebrates is a particularly dynamic environment in which trillions of commensal microorganisms exist, known as the microbiota, which plays an important role in many biological functions including growth enhancement, nutrition, development, and metabolism ( 1 , 2 ). Recently, the microbiota has been found to be closely related to the host’s immune system, as it induces the occurrence of immune responses and enhances immune susceptibility ( 3 ).…”

Section: Introductionmentioning

confidence: 99%

“…In response, the host mucosal immune system has evolved multiple means to maintain its symbiotic relationship with the microbiota ( 4 ). Unlike invertebrates, teleost fish have evolved both innate and adaptive immunity due to evolutionary pressures and can therefore protect themselves against pathogens residing in the aquatic environment and maintain mucosal microbiota homeostasis ( 2 , 5 ). Given the uniqueness and complexity of the living environment of teleost, the mucosal tissues on the surface of these organisms are the first to contact the pathogen and are therefore the first line of defense against pathogen invasion.…”

Section: Introductionmentioning

confidence: 99%

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Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection

Meng

Ding

et al. 2021

Front. Immunol.

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The crosstalk between the immune system and microbiota drives an amazingly complex mutualistic symbiosis. In mammals, the upper respiratory tract acts as a gateway for pathogen invasion, and the dynamic interaction between microbiota and mucosal immunity on its surface can effectively prevent disease development. However, the relationship between virus-mediated mucosal immune responses and microbes in lower vertebrates remains uncharacterized. In this study, we successfully constructed an infection model by intraperitoneally injecting common carp (Cyprinus carpio) with spring viremia of carp virus (SVCV). In addition to the detection of the SVCV in the nose and pharynx of common carp, we also identified obvious histopathological changes following viral infection. Moreover, numerous immune-related genes were significantly upregulated in the nose and pharynx at the peak of SVCV infection, after which the expression levels decreased to levels similar to those of the control group. Transcriptome sequencing results revealed that pathways associated with bacterial infection in the Toll-like receptor pathway and the Nod-like receptor pathway were activated in addition to the virus-related Rig-I-like receptor pathway after SVCV infection, suggesting that viral infection may be followed by opportunistic bacterial infection in these mucosal tissues. Using 16S rRNA gene sequencing, we further identified an upward trend in pathogenic bacteria on the mucosal surface of the nose and pharynx 4 days after SVCV infection, after which these tissues eventually reached new homeostasis. Taken together, our results suggest that the dynamic interaction between mucosal immunity and microbiota promotes the host to a new ecological state.

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“…Teleosts have evolved both innate and adaptive immune systems to provide protection against pathogen invasion and tissue damage through a variety of defense responses including the induction of interferons (IFNs), inflammatory cytokines, chemokines, and the activation of cell death pathways [1][2][3]. The innate immunity has been demonstrated as the first line in the host immune defense, which is initiated by the recognition of pathogen-associated molecular patterns (PAMPs) or damage-associated molecular patterns (DAMPs) through a series of receptors termed pattern recognition receptors (PRRs) including toll-like receptors (TLRs), nucleotide-binding oligomerization domain (NOD)like receptors (NLRs), retinoic acid inducible gene I (RIG-I)-like receptors (RLRs), C-type lectin receptors (CLRs), and absent in melanoma 2 (AIM2)-like receptors (ALRs), which finally activate the host immune response through an interaction with the downstream signaling molecules [4,5].…”

Section: Introductionmentioning

confidence: 99%

RIP3 Associates with RIP1, TRIF, MAVS, and Also IRF3/7 in Host Innate Immune Signaling in Large Yellow Croaker Larimichthys crocea

Zou

Liu

et al. 2021

Antibiotics

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Receptor-interacting protein 3 (RIP3) has been demonstrated to be a key regulator not only in cell death pathways including apoptosis and necroptosis but also in inflammation and host immune responses. In this study, a RIP3 ortholog named Lc-RIP3 is identified in large yellow croaker (Larimichthys crocea). The open reading frame (ORF) of Lc-RIP3 is 1524 bp long and encodes a protein of 507 amino acids (aa). The deduced Lc-RIP3 protein has an N-terminal kinase domain and a C-terminal RHIM domain, and the genome organization of Lc-RIP3 is conserved in teleosts with 12 exons and 11 introns but is different from that in mammals, which comprises 10 exons and 9 introns. Confocal microscopy revealed that Lc-RIP3 is a cytosolic protein. The expression analysis at the mRNA level indicated that Lc-RIP3 is ubiquitously distributed in various tissues/organs, and could be up-regulated under poly I:C, LPS, PGN, and Pseudomonas plecoglossicida stimulation in vivo. Notably, Lc-RIP3 could induce NF-κB but not IRF3 activation. In addition, Lc-RIP3 co-expression with Lc-TRIF, Lc-MAVS, or Lc-IRF3 significantly abolishes the activation of NF-κB but enhances the induction of IRF3 activity. Moreover, NF-κB activity could be up-regulated when Lc-RIP3 is co-expressed with Lc-RIP1 or Lc-IRF7. These results collectively indicate that Lc-RIP3 acts as an important regulator in host innate immune signaling in teleosts.

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Commensal bacteria‐immunity crosstalk shapes mucosal homeostasis in teleost fish

Cited by 62 publications

References 261 publications

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses

Teleost swim bladder, an ancient air-filled organ that elicits mucosal immune responses

Dynamic Interaction Between Mucosal Immunity and Microbiota Drives Nose and Pharynx Homeostasis of Common Carp (Cyprinus carpio) After SVCV Infection

RIP3 Associates with RIP1, TRIF, MAVS, and Also IRF3/7 in Host Innate Immune Signaling in Large Yellow Croaker Larimichthys crocea

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