The noncoding small RNA SsrA is released by Vibrio fischeri and modulates critical host responses

Plos Biology. Published: November 3, 2020

Abstract

The regulatory noncoding small RNAs (sRNAs) of bacteria are key  elements influencing gene expression; however, there has been little  evidence that beneficial bacteria use these molecules to communicate  with their animal hosts. We report here that the bacterial sRNA SsrA  plays an essential role in the light-organ symbiosis between Vibrio fischeri and the squid Euprymna scolopes. The symbionts load SsrA into outer membrane vesicles, which are  transported specifically into the epithelial cells surrounding the  symbiont population in the light organ. 共生体将SsrA加载到外膜囊泡中，外膜囊泡被特异性转运到发光器官中共生菌群体周围的上皮细胞中。 Although an SsrA-deletion mutant (ΔssrA) colonized the host to a normal level after 24 h, it  produced only 2/10 the luminescence per bacterium, and its persistence  began to decline by 48 h. The host’s response to colonization by the ΔssrA strain was also abnormal: the epithelial cells underwent premature  swelling, 皮细胞过早肿胀 and host robustness was reduced. Most notably, when colonized  by the ΔssrA strain, the light organ differentially  up-regulated 10 genes, including several encoding heightened  immune-function or antimicrobial activities. This study reveals the  potential for a bacterial symbiont’s sRNAs not only to control its own  activities but also to trigger critical responses promoting homeostasis  in its host. In the absence of this communication, there are dramatic  fitness consequences for both partners.

This symbiosis begins when a newly hatched juvenile squid is colonized by planktonic V. fischeri cells that enter pores on the surface of the nascent light organ and  proceed down a migration path ending at epithelium-lined crypt spaces (Fig 1A). Once there, the bacteria proliferate [29,30] and induce bioluminescence critical to the squid’s nocturnal behavior [31]. The initiation of this highly specific association involves a choreographed exchange of signals [32] that changes gene expression in both partners [33,34]. As a result, colonization by V. fischeri down-regulates several host antimicrobial responses, including phagocytosis [35], and the production of nitric oxide [36] and halide peroxidase [37]. Nevertheless, the pathways by which these immune adaptations are  achieved, and their importance to symbiotic homeostasis, have remained  unexplained.

Fig 1.  Symbiont noncoding RNA, SsrA, localizes within the crypt epithelium.

(A) Diagram of a juvenile squid showing the anatomical location (left) and  internal aspects (middle) of the light organ, illustrating one of its  two pairs of cea, and three entry pores (“p”) through which the  symbionts reach the migration path to internal crypts (“c”). Gray dots  inside the sinus of the cea represent symbiosis-induced trafficking of  hemocytes. (Right) Illustration of the close contact between the V. fischeri population (green) and the light-organ epithelial cells in a crypt. (B) Relative proportions of types of V. fischeri RNAs present in squid H-lymph or in the RNA cargo of OMVs (S1 Data). (C) Volcano-plot representation of fold-change in gene expression (log2FC) of the RNA cargo in OMVs produced by WT or the ssrA-deletion mutant ΔssrA strain; the only significant difference in RNA content is the presence (in WT) or absence (in ΔssrA) of SsrA. Transcripts with evidence for significant differential expression (FDR < 0.05) are colored in red (S1 Data). (D) Localization of symbiont SsrA transcript by confocal microscopy, 24 h after colonization by WT or ΔssrA bacteria. Left: merged images with orthogonal views; other panels: images of individual labels. (E) Higher magnification of WT V. fischeri cells (green) colonizing the light organ, showing the location of SsrA  transcript (magenta) within the cytoplasm of host epithelial cells. cea, ciliated epithelial appendages; FDR, false discovery rate; H-lymph,  hemolymph; OMV, outer membrane vesicle; sRNA, small RNA; WT, wild type.

Table 1.  List of abundant small, noncoding RNAs

A small RNA for a long-lasting relationship

Nature Reviews Microbiology                         (2020)

Non-coding small RNAs (sRNAs) of bacteria regulate the expression of various bacterial functions such as metabolism, virulence and environmental stress responses, but there  has been little evidence to suggest that sRNAs have a role in  inter-kingdom communication between symbiotic bacteria and their animal  hosts. During establishment of a symbiotic relationship with their  animal hosts, beneficial bacteria must restrain the host immune system  to ensure stable colonization; however, a complete understanding of the  underlying mechanisms is lacking. Now, Moriano-Gutierrez et al. report  that a sRNA released by the bioluminescent bacterium Vibrio fischeri modulates crucial host responses in the Hawaiian bobtailed squid Euprymna scolopes, revealing a new mode of communication in beneficial animal–bacterial symbioses.

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