Volatility as a concept to understand the impact of stress on the microbiome

Authors: BASTIAANSSEN, THOMAZ - University College Cork; GURURAJAN, ANAND - University College Cork; VAN DE WOUW, MARCEL - University College Cork; MOLONEY, GERARD - University College Cork; RITZ, NATHANIEL - University College Cork; LONG-SMITH, CAITRIONA - University College Cork; WILEY, NIAMH - University College Cork; MURPHY, AMY - University College Cork; Lyte, Joshua - Josh; FOUHY, FIONA - University College Cork; STANTON, CATHERINE - University College Cork; CLAESSON, MARCUS - University College Cork; DINAN, TIMOTHY - University College Cork; DINAN, TIMOTHY - University College Cork; CRYAN, JOHN - University College Cork

Submitted to: Psychoneuroendocrinology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/3/2020
Publication Date: 12/8/2020
Citation: Bastiaanssen, T.F., Gururajan, A., Van De Wouw, M., Moloney, G.M., Ritz, N., Long-Smith, C.M., Wiley, N.C., Murphy, A.B., Lyte, J.M., Fouhy, F., Stanton, C., Claesson, M., Dinan, T., Dinan, T.G., Cryan, J.F. 2020. Volatility as a concept to understand the impact of stress on the microbiome. Psychoneuroendocrinology. https://doi.org/10.1016/j.psyneuen.2020.105047.
DOI: https://doi.org/10.1016/j.psyneuen.2020.105047

Interpretive Summary: The gut microbiota is the collection of microorganisms, including bacteria, found in the gut. As the microbiota are increasingly recognized to play important roles in affecting host (meaning, the person or animal) health, it is important to remember that the relationship between microbiota and host is mutual so that the host affects the microbiota just as the microbiota affects the host. It is therefore necessary to understand how the microbiota may change when the host is chronically stressed. Understanding how the microbiota changes before, during, and after a chronic stress may help scientists uncover microbiota populations in the gut that are linked to, or help predict, negative or positive changes in host health as a consequence of stress. In this research article, we demonstrate a new way of understanding stress-induced changes in the microbiome that are associated with changes in host measures of stress response. This new method of analyzing and interpreting microbiota changes in response to chronic stress will likely help other researchers interpret their microbiota findings through a new perspective, possibly leading to improved health of people and animals.

Technical Abstract: The microbiome-gut-brain-axis is a complex phenomenon spanning several dynamic systems in the body which can be parsed at a molecular, cellular, physiological and ecological level. A growing body of evidence indicates that this axis is particularly sensitive to the effects of stress and that it maybe relevant to how the body regulates acute and chronic stress. In classical ecology terms, compositional change of the microbial system over time is a well-studied concept. Although stress-induced changes in the composition of the microbiome have been reported, the degree of compositional change over time, which we define as volatility, has not been the subject of much scrutiny as of yet. Using a chronic psychosocial stress paradigm in mice, we report that the volatility of the microbiome significantly correlated with several central and peripheral readouts of the stress response. Furthermore, we show that the abundance of several taxa and their predicted functions at baseline were linked to volatility. This approach highlights limitations in conventional methodologies to analyse the effects of stress on the dynamic microbiome and underscores the informative value of volatility as a parameter that should be considered in all future analyses of the microbiome.