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1. An urban diet differentially alters the gut microbiome and metabolomic profiles compared with a seed diet in mourning doves

   https://doi.org/10.1152/ajpregu.00323.2021  

   Mohr, Alex E. ; Basile, Anthony J. ; Sweazea, Karen L. ( October 2022 , American Journal of Physiology-Regulatory, Integrative and Comparative Physiology)

   Urbanization influences food quality and availability for many avian species, with increased access to human refuse and food subsidies in built environments. In relation to such nutritional intakes and their presumed impact on microbes harbored in the intestinal tract and metabolic profiles of host physiological systems, our overall knowledge of the role of gut microbiome (GM) and metabolomic expression in the avian host lags far behind our understanding of mammals. Therefore, the objective of this investigation was to examine the potential differential effect of an urban modeled versus control (i.e., bird seed) diet on the GM, the metabolic profiles of plasma, liver, adipose, kidney, and muscle tissues, and circulating endotoxin and inflammatory factors in urban-caught mourning doves ( Zenaida macroura). We hypothesized that the urban diet would differently impact the profiles of the GM and tissue metabolomes and increase plasma lipopolysaccharide (LPS) and proinflammatory factors compared with animals fed a seed diet. After a 4-wk-diet period, contents of the large intestine were sequenced to profile the microbiome, metabolomic analyses were performed on plasma and tissue homogenates, and circulating LPS and inflammatory markers were assessed. The composition of the GM was significantly dissimilar between diets, with greater abundance of Erysipelatoclostridiaceae, Sanguibacteraceae, Oribacterium, and Sanguibacter and decreased circulating LPS in the urban-fed birds. These differences were largely not reflected in the surveyed metabolomes and plasma inflammatory markers. This research supports the notion that the microbial composition in urban doves is impacted by diet, though may only weakly associate with host physiology. 

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2. The gut microbiome influences host diet selection behavior

   https://doi.org/10.1073/pnas.2117537119  

   Trevelline, Brian K. ; Kohl, Kevin D. ( April 2022 , Proceedings of the National Academy of Sciences)

   Diet selection is a fundamental aspect of animal behavior with numerous ecological and evolutionary implications. While the underlying mechanisms are complex, the availability of essential dietary nutrients can strongly influence diet selection behavior. The gut microbiome has been shown to metabolize many of these same nutrients, leading to the untested hypothesis that intestinal microbiota may influence diet selection. Here, we show that germ-free mice colonized by gut microbiota from three rodent species with distinct foraging strategies differentially selected diets that varied in macronutrient composition. Specifically, we found that herbivore-conventionalized mice voluntarily selected a higher protein:carbohydrate (P:C) ratio diet, while omnivore- and carnivore-conventionalized mice selected a lower P:C ratio diet. In support of the long-standing hypothesis that tryptophan—the essential amino acid precursor of serotonin—serves as a peripheral signal regulating diet selection, bacterial genes involved in tryptophan metabolism and plasma tryptophan availability prior to the selection trial were significantly correlated with subsequent voluntary carbohydrate intake. Finally, herbivore-conventionalized mice exhibited larger intestinal compartments associated with microbial fermentation, broadly reflecting the intestinal morphology of their donor species. Together, these results demonstrate that gut microbiome can influence host diet selection behavior, perhaps by mediating the availability of essential amino acids, thereby revealing a mechanism by which the gut microbiota can influence host foraging behavior. 

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3. The role of the microbiome in the neurobiology of social behaviour

   https://doi.org/10.1111/brv.12603  

   Sarkar, Amar ; Harty, Siobhán ; Johnson, Katerina V. ‐A. ; Moeller, Andrew H. ; Carmody, Rachel N. ; Lehto, Soili M. ; Erdman, Susan E. ; Dunbar, Robin I. M. ; Burnet, Philip W. J. ( May 2020 , Biological Reviews)

   Microbes colonise all multicellular life, and the gut microbiome has been shown to influence a range of host physiological and behavioural phenotypes. One of the most intriguing and least understood of these influences lies in the domain of the microbiome's interactions with host social behaviour, with new evidence revealing that the gut microbiome makes important contributions to animal sociality. However, little is known about the biological processes through which the microbiome might influence host social behaviour. Here, we synthesise evidence of the gut microbiome's interactions with various aspects of host sociality, including sociability, social cognition, social stress, and autism. We discuss evidence of microbial associations with the most likely physiological mediators of animal social interaction. These include the structure and function of regions of the ‘social' brain (the amygdala, the prefrontal cortex, and the hippocampus) and the regulation of ‘social’ signalling molecules (glucocorticoids including corticosterone and cortisol, sex hormones including testosterone, oestrogens, and progestogens, neuropeptide hormones such as oxytocin and arginine vasopressin, and monoamine neurotransmitters such as serotonin and dopamine). We also discuss microbiome‐associated host genetic and epigenetic processes relevant to social behaviour. We then review research on microbial interactions with olfaction in insects and mammals, which contribute to social signalling and communication. Following these discussions, we examine evidence of microbial associations with emotion and social behaviour in humans, focussing on psychobiotic studies, microbe–depression correlations, early human development, autism, and issues of statistical power, replication, and causality. We analyse how the putative physiological mediators of the microbiome–sociality connection may be investigated, and discuss issues relating to the interpretation of results. We also suggest that other candidate molecules should be studied, insofar as they exert effects on social behaviour and are known to interact with the microbiome. Finally, we consider different models of the sequence of microbial effects on host physiological development, and how these may contribute to host social behaviour.

    

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4. Reflections on the Use of an Invertebrate Chordate Model System for Studies of Gut Microbial Immune Interactions

   https://doi.org/10.3389/fimmu.2021.642687  

   Liberti, Assunta ; Natarajan, Ojas ; Atkinson, Celine Grace ; Sordino, Paolo ; Dishaw, Larry J. ( February 2021 , Frontiers in Immunology)

   null (Ed.)

   The functional ecology of the gastrointestinal tract impacts host physiology, and its dysregulation is at the center of various diseases. The immune system, and specifically innate immunity, plays a fundamental role in modulating the interface of host and microbes in the gut. While humans remain a primary focus of research in this field, the use of diverse model systems help inform us of the fundamental principles legislating homeostasis in the gut. Invertebrates, which lack vertebrate-style adaptive immunity, can help define conserved features of innate immunity that shape the gut ecosystem. In this context, we previously proposed the use of a marine invertebrate, the protochordate Ciona robusta , as a novel tractable model system for studies of host-microbiome interactions. Significant progress, reviewed herein, has been made to fulfill that vision. We examine and review discoveries from Ciona that include roles for a secreted immune effector interacting with elements of the microbiota, as well as chitin-rich mucus lining the gut epithelium, the gut-associated microbiome of adults, and the establishment of a large catalog of cultured isolates with which juveniles can be colonized. Also discussed is the establishment of methods to rear the animals germ-free, an essential technology for dissecting the symbiotic interactions at play. As the foundation is now set to extend these studies into the future, broadening our comprehension of how host effectors shape the ecology of these microbial communities in ways that establish and maintain homeostasis will require full utilization of “multi-omics” approaches to merge computational sciences, modeling, and experimental biology in hypothesis-driven investigations. 

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5. Nod‐like receptors are critical for gut–brain axis signalling in mice

   https://doi.org/10.1113/JP278640  

   Pusceddu, Matteo M. ; Barboza, Mariana ; Keogh, Ciara E. ; Schneider, Melinda ; Stokes, Patricia ; Sladek, Jessica A. ; Kim, Hyun Jung D. ; Torres‐Fuentes, Cristina ; Goldfild, Lily R. ; Gillis, Shane E. ; et al ( November 2019 , The Journal of Physiology)

   Nucleotide binding oligomerization domain (Nod)‐like receptors regulate cognition, anxiety and hypothalamic–pituitary–adrenal axis activation.

   Nod‐like receptors regulate central and peripheral serotonergic biology.

   Nod‐like receptors are important for maintenance of gastrointestinal physiology.

   Intestinal epithelial cell expression of Nod1 receptors regulate behaviour.

   Gut–brain axis signalling is critical for maintaining health and homeostasis. Stressful life events can impact gut–brain signalling, leading to altered mood, cognition and intestinal dysfunction. In the present study, we identified nucleotide binding oligomerization domain (Nod)‐like receptors (NLR), Nod1 and Nod2, as novel regulators for gut–brain signalling. NLR are innate immune pattern recognition receptors expressed in the gut and brain, and are important in the regulation of gastrointestinal physiology. We found that mice deficient in both Nod1 and Nod2 (NodDKO) demonstrate signs of stress‐induced anxiety, cognitive impairment and depression in the context of a hyperactive hypothalamic–pituitary–adrenal axis. These deficits were coupled with impairments in the serotonergic pathway in the brain, decreased hippocampal cell proliferation and immature neurons, as well as reduced neural activation. In addition, NodDKO mice had increased gastrointestinal permeability and altered serotonin signalling in the gut following exposure to acute stress. Administration of the selective serotonin reuptake inhibitor, fluoxetine, abrogated behavioural impairments and restored serotonin signalling. We also identified that intestinal epithelial cell‐specific deletion of Nod1 (VilCre⁺Nod1^f/f), but not Nod2, increased susceptibility to stress‐induced anxiety‐like behaviour and cognitive impairment following exposure to stress. Together, these data suggest that intestinal epithelial NLR are novel modulators of gut–brain communication and may serve as potential novel therapeutic targets for the treatment of gut–brain disorders.

    

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