Host-microbe interactions and the behavior of Caenorhabditis elegans

Abstract

Microbes are ubiquitous in the natural environment of Caenorhabditis elegans. Bacteria serve as a food source for C. elegans but may also cause infection in the nematode host. The sensory nervous system of C. elegans detects diverse microbial molecules, ranging from metabolites produced by broad classes of bacteria to molecules synthesized by specific strains of bacteria. Innate recognition through chemosensation of bacterial metabolites or mechanosensation of bacteria can induce immediate behavioral responses. The ingestion of nutritive or pathogenic bacteria can modulate internal states that underlie long-lasting behavioral changes. Ingestion of nutritive bacteria leads to learned attraction and exploitation of the bacterial food source. Infection, which is accompanied by activation of innate immunity, stress responses, and host damage, leads to the development of aversive behavior. The integration of a multitude of microbial sensory cues in the environment is shaped by experience and context. Genetic, chemical, and neuronal studies of C. elegans behavior in the presence of bacteria have defined neural circuits and neuromodulatory systems that shape innate and learned behavioral responses to microbial cues. These studies have revealed the profound influence that host-microbe interactions have in governing the behavior of this simple animal host.

What can a worm learn in a bacteria-rich habitat?

“…The border and the texture of a bacterial lawn may also generate mechanical stimulation to moving worms. These bacteriaderived sensory cues act in a combinatorial manner to elicit behavioral responses in C. elegans [ (Bargmann, Hartwieg, & Horvitz, 1993;Brandt & Ringstad, 2015;Bretscher et al, 2008;Calhoun et al, 2015;Cheung et al, 2005;Flavell et al, 2013;Kim & Flavell, 2020;Gramstrup Petersen et al, 2013;Gray et al, 2004;Ha et al, 2010;Hallem et al, 2011;Hao et al, 2018;Harris et al, 2019;Meisel, Panda, Mahanti, Schroeder, & Kim, 2014;Ooi & Prahlad, 2017;Pradel et al, 2007;Reddy et al, 2011;Rhoades et al, 2019;Sawin, Ranganathan, & Horvitz, 2000;Tran et al, 2017) and the references therein]. The diversity of the sensory cues is consistent with multiple signaling pathways that are identified to mediate bacteria-worm interactions.…”

“…The virulence of the bacteria, as well as several bacteria-derived chemicals act together to repel the worms from the lawn. The mechanisms underlying the changes in behavior and physiology of the worms over this process are separately reviewed (Hoffman & Aballay, 2019;Kim & Flavell, 2020;Kim & Ewbank, 2018;.…”

Neuromodulators: an essential part of survival

“…Remarkably, C. elegans is subject to signaling not only from its self-synthesized OA, but also from OA or OA-like compounds secreted by certain bacteria or other C. elegans, respectively. In this issue, Kim and Flavell (2020) highlight the recent findings from the Sengupta lab (O'Donnell, Fox, Chao, Schroeder, & Sengupta, 2020) on how OA produced by commensal bacteria alters C. elegans behavior and internal state. Cheon et al (2020; this issue) and Muirhead and Srinivasan (2020; this issue) also review how starved larvae produce the OA-like small molecule osas#9, an ascaroside component of the worm-secreted pheromone blend, which is then sensed by nociceptive ASH neurons in adults to initiate their avoidance behavior (Chute et al, 2019).…”

“…The profound influence of neuromodulators on behavior, metabolism, and overall physiology is a common thread throughout this issue (Cheon, Hwang, & Kim, 2020;Honer et al, 2020;Kim & Flavell, 2020;Kim, Lee, Kim, & Lee, 2020;Liang, McKinnon, & Rankin, 2020;Liu & Zhang, 2020;Muirhead & Srinivasan, 2020;Prahlad, 2020;Srinivasan, 2020;Takeishi, Takagaki, & Kuhara, 2020;Yang, Lee, Yim, & Lee, 2020). In this perspective, we will focus on the roles of monoamines and neuropeptides in C. elegans survival.…”

“…Caenorhabditis elegans is a bacterivore, and the bacteria encountered by the animal range from highly nutritious to poorly nutritious and outright pathogenic (see Kim & Flavell, 2020;this issue). Interestingly, OA also suppresses aversive behaviors (Guo et al, 2015;Mills et al, 2012) to prioritize feeding.…”