The role of the commensal microbiota in adaptive and maladaptive stressor-induced immunomodulation

Abstract

Over the past decade, it has become increasingly evident that there are extensive bidirectional interactions between the body and its microbiota. These interactions are evident during stressful periods, where it is recognized that commensal microbiota community structure is significantly changed. Many different stressors, ranging from early life stressors to stressors administered during adulthood, lead to significant, community-wide differences in the microbiota. The mechanisms through which this occurs are not yet known, but it is known that commensal microbes can recognize, and respond to, mammalian hormones and neurotransmitters, including those that are involved with the physiological response to stressful stimuli. In addition, the physiological stress response also changes many aspects of gastrointestinal physiology that can impact microbial community composition. Thus, there are many routes through which microbial community composition might be disrupted during stressful periods. The implications of these disruptions in commensal microbial communities for host health are still not well understood, but the commensal microbiota have been linked to stressor-induced immunopotentiation. The role of the microbiota in stressor-induced immunopotentiation can be adaptive, such as when these microbes stimulate innate defenses against bacterial infection. However, the commensal microbiota can also lead to maladaptive immune responses during stressor-exposure. This is evident in animal models of colonic inflammation where stressor exposure increases the inflammation through mechanisms involving the microbiota. It is likely that during stressor exposure, immune cell functioning is regulated by combined effects of both neurotransmitters/hormones and commensal microbes. Defining this regulation should be a focus of future studies.

Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota

“…However, perturbing the GI environment can initiate a vicious cycle whereby consequent deleterious shifts in the gut microbiota, known as dysbiosis, exacerbate decrements to GI physiology that maintain dysbiosis. Dysbiosis has been associated with transient health decrements including GI permeability and inflammation ( Cani et al, 2012 ; Wells et al, 2017 ), increased susceptibility to illness and infection ( Zanella Terrier et al, 2014 ; Mackos et al, 2017 ), and psychological impairments ( Cryan and Dinan, 2012 ; Foster and McVey Neufeld, 2013 ). Further, dysbiosis has been associated with multiple chronic diseases such as obesity and associated cardiometabolic diseases ( Turnbaugh et al, 2009 ), inflammatory bowel disease ( Sartor, 2008 ), colon cancer ( O’Keefe, 2016 ), autoimmune diseases ( Vaahtovuo et al, 2008 ; Russell et al, 2012 ), and psychological disorders ( Luna and Foster, 2015 ; Leclercq et al, 2016 ) among others ( Tremaroli and Backhed, 2012 ).…”

“…It is increasingly recognized that stress modulates gut microbiota community structure and activity, and may be one causal factor in dysbiosis ( Mackos et al, 2017 ). Stress can be defined as a disruption in homeostasis due to environmental, physical, or psychological stimuli (i.e., stressors) that elicits adaptive physiological and behavioral responses to restore homeostasis (i.e., the stress response) ( Glaser and Kiecolt-Glaser, 2005 ).…”

Microbiota of newborn meconium is associated with maternal anxiety experienced during pregnancy

“…Recent animal models suggest that newborn gut microbiota might contribute to the link between maternal stress in pregnancy and infant health and neurodevelopment (Jašarević, Howerton et al, ; Jašarević, Rodgers et al, ; Mackos, Maltz, & Bailey, ), which have challenged the “sterile womb paradigm”. Those studies contributed to a growing consensus that commensal bacteria are present in the intrauterine environment and may influence the bacterial colonization of babies before birth (DiGiulio et al, ; Jiménez et al, ; Rautava, Collado, Salminen, & Isolauri, ; Satokari, Grönroos, Laitinen, Salminen, & Isolauri, ) or during the delivery when the baby goes through the birth canal (Jašarević, Rodgers et al, ).…”

Dietary Heat-Killed <i>Lactobacillus brevis</i> SBC8803 Attenuates Chronic Sleep Disorders Induced by Psychophysiological Stress in Mice

“…Stress can be defined as a disruption in homeosta- sis due to environmental, physical or psychological stimuli that elicit adaptive physiological and behavioral responses to restore homeostasis (17). Stress modulates the structure and activity of the gut microbiota, which might be one cause of dysbiosis (18,19).…”