Microbial colonization promotes model cockroach gut tissue growth and development. (August 2021)

• Record Type: Journal Article
• Authors: Jahnes, Benjamin C.; Poudel, Keyshap; Staats, Amelia M.; Sabree, Zakee L.
• Is Part Of: Journal of insect physiology. Volume 133(2021)
• Publication Date: 2021-08
• Subjects: Periplaneta americana -- Gut development -- Microbiome -- Cockroach -- Gut epithelium -- Germ free; Insects -- Physiology -- Periodicals; Insectes -- Physiologie -- Périodiques; Insects -- Physiology; Periodicals; 571.157
• DOI: 10.1016/j.jinsphys.2021.104274
• Languages: English
• ISSNs: 0022-1910

Abstract

Graphical abstract: Highlights: Elimination of gut microbiota results in a highly reduced gut physiology. A single coprophagic opportunity can partially restore normal gut physiology. Posterior gut tissues house the most microbes and are sensitive to their absence. Gut commensals have distinct developmental impacts on midgut and hindgut tissues. Abstract: Background: Digestive tissues are essential for diet processing and nutrient accessibility, especially in omnivores, and these functions occur despite and in collaboration with dynamic microbial communities that reside within and upon these tissues. Prolonged host development and reduced digestive tissue sizes have been observed in germ-free animals, and normal host phenotypes were recovered following the re-introduction of typical gut microbiomes via coprophagy. Results: High-resolution histological analyses of Periplaneta americana cockroach digestive tissues revealed that total prevention of microbial colonization of the gut had severe impacts on the growth and development of gut tissues, especially the posterior midgut and anterior hindgut subcompartments that are expected to be colonized and inhabited by the greatest number of bacteria. Juveniles that were briefly exposed to normal gut microbiota exhibited a partial gut morphological recovery, suggesting that a single inoculation was insufficient. These data highlight gut microbiota as integral to normal growth and development of tissues they are in direct contact with and, more broadly, the organism in which they reside. Conclusions: We draw on these data, host life history traits (i.e. multigenerational cohousing, molting, and filial coprophagy and exuvia feeding), and previous studies to suggest a host developmental model in which gut tissues reflect a conflict-collaboration dynamic where 1) nutrient-absorptive anterior midgut tissues are in competition with transient and resident bacteria for easily assimilable dietary nutrients and whose growth is least-affected by the presence of gut bacteria and 2) posterior midgut, anterior hindgut, and to a lesser degree, posterior hindgut tissues are significantly impacted by gut bacterial presence because they are occupied by the greatest number of bacteria and the host is relying upon, and thus collaborating with, them to assist with complex polysaccharide catabolism processing and nutrient provisioning (i.e. short-chain fatty acids).