Reciprocal Interactions between Nematodes and Their Microbial Environments

Abstract

Parasitic nematode infections are widespread in nature, affecting humans as well as wild, companion, and livestock animals. Most parasitic nematodes inhabit the intestines of their hosts living in close contact with the intestinal microbiota. Many species also have tissue migratory life stages in the absence of severe systemic inflammation of the host. Despite the close coexistence of helminths with numerous microbes, little is known concerning these interactions. While the environmental niche is considerably different, the free-living nematode Caenorhabditis elegans (C. elegans) is also found amongst a diverse microbiota, albeit on decaying organic matter. As a very well characterized model organism that has been intensively studied for several decades, C. elegans interactions with bacteria are much more deeply understood than those of their parasitic counterparts. The enormous breadth of understanding achieved by the C. elegans research community continues to inform many aspects of nematode parasitology. Here, we summarize what is known regarding parasitic nematode-bacterial interactions while comparing and contrasting this with information from work in C. elegans. This review highlights findings concerning responses to bacterial stimuli, antimicrobial peptides, and the reciprocal influences between nematodes and their environmental bacteria. Furthermore, the microbiota of nematodes as well as alterations in the intestinal microbiota of mammalian hosts by helminth infections are discussed.

Keywords: antibiotic resistance; antimicrobial peptides; helminth; microbiota; nematode.

Figure 1

Diverse influences of nematodes on the gut microbiota of their hosts.

Figure 2

Mutual influences of intestinal nematodes and host-gut bacteria. Establishment and persistence of intestinal nematodes in the host's gut are affected by bacterial communities and lead to substantial changes of the gut microbiota. Here, nematode-microbiota interactions and their impact on the host immune response and physiology are exemplified. (1) Egg hatching: Interaction of eggs with the intestinal microbiota is needed for some species, enabling larvae to hatch. (2) Mucosal immune response: Attachment to the epithelium and tissue migratory phase might lead to bacterial translocation and manipulation of immune responses. The anti-helminth immune response is predominantly a T helper type 2 response. (3) Gut physiology: Immune responses induce changes in gut physiology via induction of goblet cell hyperplasia, mucus production, and epithelial turnover, leading to changes in the host microbiota and its metabolome. Specific subsets of bacteria directly influence host physiology through their metabolic activities (e.g., short chain fatty acids-producing bacteria). (4) Microbiota composition: Intestinal nematodes modify intestinal microbial communities via different mechanisms: a) directly via secretion of antibacterial molecules and/or excretory/secretory products, b) indirectly by metabolic and physiologic shifts influencing the gut milieu. Chronic infections often lead to reduction in bacterial diversity and outgrowth of specific bacterial species beneficial for parasite survival. (5) Host metabolism: Intestinal nematodes modify host metabolism and nutrient uptake, e.g., alter amino acid, fatty acid, and carbohydrate metabolism, with subsequent influence on gut physiology, immune reactivity, and intestinal microbiota composition. (6) Nematode's microbiota: Nematode-associated bacterial communities might reflect the host microbiota and may also serve as transmission vehicles for pathogenic bacteria. Th2 cell, T helper type 2 cell; AAM, alternatively activated macrophage.