Critical symbiont signals drive both local and systemic changes in diel and developmental host gene expression

Abstract

The colonization of an animal's tissues by its microbial partners creates networks of communication across the host's body. We used the natural binary light-organ symbiosis between the squid Euprymna scolopes and its luminous bacterial partner, Vibrio fischeri, to define the impact of colonization on transcriptomic networks in the host. A night-active predator, E. scolopes coordinates the bioluminescence of its symbiont with visual cues from the environment to camouflage against moon and starlight. Like mammals, this symbiosis has a complex developmental program and a strong day/night rhythm. We determined how symbiont colonization impacted gene expression in the light organ itself, as well as in two anatomically remote organs: the eye and gill. While the overall transcriptional signature of light organ and gill were more alike, the impact of symbiosis was most pronounced and similar in light organ and eye, both in juvenile and adult animals. Furthermore, the presence of a symbiosis drove daily rhythms of transcription within all three organs. Finally, a single mutation in V. fischeri-specifically, deletion of the lux operon, which abrogates symbiont luminescence-reduced the symbiosis-dependent transcriptome of the light organ by two-thirds. In addition, while the gills responded similarly to light-organ colonization by either the wildtype or mutant, luminescence was required for all of the colonizationassociated transcriptional responses in the juvenile eye. This study defines not only the impact of symbiont colonization on the coordination of animal transcriptomes, but also provides insight into how such changes might impact the behavior and ecology of the host. squid-vibrio | symbiosis | development | daily rhythm | bioluminescence

Shining light on microbial signaling to distant organs

“…Moriano-Gutierrez et al (2) observed that the transcriptional profiles of juvenile and adult animals were relatively similar in the gill and more different in the light organ; the largest separation occurring between samples was observed in the eye. This observation suggests that the eye has significant postnatal developmental regulation, although some caution should be made since the data are based on relatively few replicates.…”

“…A central goal for all symbiotic research is to delineate whether, and how, the symbiosis signals to distal organs of the host. In PNAS, by using the binary squid-vibrio model and isogenic bacterial mutants, Moriano-Gutierrez et al (2) demonstrate that light produced by the bacteria has a dramatic impact on the transcriptome in the light organ as well as the eye, whereas the response in the gills is independent of the bioluminescence produced by V. fischeri.…”

Tracking the cargo of extracellular symbionts into host tissues with correlated electron microscopy and nanoscale secondary ion mass spectrometry imaging

“…These microbe‐associated molecular patterns (MAMPs) are presented to the host crypt epithelia as either freely exported molecules (Koropatnick et al, ) or molecules delivered in outer membrane vesicles (OMVs; Aschtgen et al, ; Aschtgen, Wetzel, Goldman, McFall‐Ngai, & Ruby, ). Further, from the crypt spaces, the symbionts induce transcriptomic changes in remote tissues, such as the eyes and gills (Moriano‐Gutierrez et al, ).…”

“…Whereas host receptor/symbiont ligand interactions (e.g., MAMPs and pattern recognition receptors) driving these specific developmental events have been extensively studied (for reviews, see McFall-Ngai, Heath-Heckman, Gillette, Peyer, & Harvie, 2012;Nyholm & Graf, 2012), many other communication networks have been suggested by "-omics" studies (Chun et al, 2008;Kremer et al, 2013;Moriano-Gutierrez et al, 2019;Wier et al, 2010). How host communication is mediated to drive development and maturation of these networks is currently unknown.…”

HbtR, a heterofunctional homolog of the virulence regulator TcpP, facilitates the transition between symbiotic and planktonic lifestyles inVibrio fischeri

“…Light production by V. fischeri is a crucial factor in the mutualistic symbiosis it forms within the light organ of the Hawaiian bobtail squid, Euprymna scolopes (7–9). Juvenile E. scolopes become colonized with V. fischeri shortly after hatching into seawater containing this bacterium (10).…”