Coral mucus rapidly induces chemokinesis and genome-wide transcriptional shifts toward early pathogenesis in a bacterial coral pathogen

Cherry Gao,Roman Stocker,Vicente I Fernandez,Janelle R Thompson,Jean-Baptiste Raina,Kevin Penn,Melissa Garren,Justin R Seymour

doi:10.1038/s41396-021-01024-7

Abstract

Elevated seawater temperatures have contributed to the rise of coral disease mediated by bacterial pathogens, such as the globally distributed Vibrio coralliilyticus, which utilizes coral mucus as a chemical cue to locate stressed corals. However, the physiological events in the pathogens that follow their entry into the coral host environment remain unknown. Here, we present simultaneous measurements of the behavioral and transcriptional responses of V. coralliilyticus BAA-450 incubated in coral mucus. Video microscopy revealed a strong and rapid chemokinetic behavioral response by the pathogen, characterized by a two-fold increase in average swimming speed within 6 min of coral mucus exposure. RNA sequencing showed that this bacterial behavior was accompanied by an equally rapid differential expression of 53% of the genes in the V. coralliilyticus genome. Specifically, transcript abundance 10 min after mucus exposure showed upregulation of genes involved in quorum sensing, biofilm formation, and nutrient metabolism, and downregulation of flagella synthesis and chemotaxis genes. After 60 min, we observed upregulation of genes associated with virulence, including zinc metalloproteases responsible for causing coral tissue damage and algal symbiont photoinactivation, and secretion systems that may export toxins. Together, our results suggest that V. coralliilyticus employs a suite of behavioral and transcriptional responses to rapidly shift into a distinct infection mode within minutes of exposure to the coral microenvironment.

Highlights

Coral reefs are declining worldwide due to rising sea surface temperatures and increasing prevalence of coral disease outbreaks [1,2,3]
We have reported a rapid behavioral and transcriptional response of V. coralliilyticus to coral mucus exposure, which led to a two-fold increase in swimming speed and significant differential expression of 53% of the genes in the genome within 10 min
Our findings identify coral mucus as a potential chemical signal that induces pathogens to prepare for host colonization and infection

Summary

Introduction

Coral reefs are declining worldwide due to rising sea surface temperatures and increasing prevalence of coral disease outbreaks [1,2,3]. The bacterial pathogen uses chemotaxis to target chemical signatures present in the mucus of stressed corals [9]. V. coralliilyticus displays chemokinesis, which is the ability to change swimming speed in response to a change in chemical concentration, to potentially enable faster environmental exploration in the presence of its coral host mucus [9, 10]. To study chemokinesis independently from chemotaxis, we conducted our experiments in the absence of chemical gradients This represents the first investigation to couple behavioral and transcriptomic analyses to decipher the mechanisms promoting coral infection. We show that behavioral and transcriptional responses occur concomitantly over a surprisingly rapid timescale of only minutes, highlighting the agility of the pathogens in seizing what are likely to be limited windows of opportunity [25] to target and infect their host

Materials and methods

Experimental setup

Results

Discussion

Compliance with ethical standards