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1. A gut feeling: Microbiome-brain-immune interactions modulate social and affective behaviors

   https://doi.org/doi.org/10.1016/j.yhbeh.2018.02.001  

   Sylvia, Kristyn and (April 2018, Brain, behavior, and immunity)

   The expression of a wide range of social and affective behaviors, including aggression and investigation, as well as anxiety- and depressive-like behaviors, involves interactions among many different physiological systems, including the neuroendocrine and immune systems. Recent work suggests that the gut microbiome may also play a critical role in modulating behavior and likely functions as an important integrator across physiological systems. Microbes within the gut may communicate with the brain via both neural and humoral pathways, providing numerous avenues of research in the area of the gut-brain axis. We are now just beginning to understand the intricate relationships among the brain, microbiome, and immune system and how they work in concert to influence behavior. The effects of different forms of experience (e.g., changes in diet, immune challenge, and psychological stress) on the brain, gut microbiome, and the immune system have often been studied independently. Though because these systems do not work in isolation, it is essential to shift our focus to the connections among them as we move forward in our investigations of the gut-brain axis, the shaping of behavioral phenotypes, and the possible clinical implications of these interactions. This review summarizes the recent progress the field has made in understanding the important role the gut microbiome plays in the modulation of social and affective behaviors, as well as some of the intricate mechanisms by which the microbiome may be communicating with the brain and immune system. 

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2. Immune Gene Expression Covaries with Gut Microbiome Composition in Stickleback

   https://doi.org/10.1128/mBio.00145-21  

   Fuess, Lauren E.; den Haan, Stijn; Ling, Fei; Weber, Jesse N.; Steinel, Natalie C.; Bolnick, Daniel I. (January 2021, mBio)

   Rawls, John F.; McFall-Ngai, Margaret J. (Ed.)

   ABSTRACT Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions, as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However, few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here, we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immune genes. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated with host gene expression. These families were all tightly correlated with host expression of immune genes and processes, falling into one of three categories—those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with the abundance of these taxa, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition. IMPORTANCE Here, we document associations between host gene expression and gut microbiome composition in a nonmammalian vertebrate species. We highlight associations between expression of immune genes and both microbiome diversity and abundance of specific microbial taxa. These findings support other findings from model systems which have suggested that gut microbiome composition and host immunity are intimately linked. Furthermore, we demonstrate that these correlations are truly systemic; the gene expression detailed here was collected from an important fish immune organ (the head kidney) that is anatomically distant from the gut. This emphasizes the systemic impact of connections between gut microbiota and host immune function. Our work is a significant advancement in the understanding of immune-microbiome links in nonmodel, natural systems. 

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3. An early-life perspective is needed to explain the impact of gut microbiota on wild vertebrate phenotypes

   https://doi.org/10.1242/jeb.250130  

   Fontaine, Samantha S; Trevelline, Brian K (July 2025, Journal of Experimental Biology)

   Vertebrates house dense and diverse communities of microorganisms in their gastrointestinal tracts. These communities shape host physiological and ecological phenotypes in diverse ways, with implications for animal fitness in nature. Exposure to microbes during the earliest stages of life is particularly important because, during critical developmental windows, the microbiome is exceptionally plastic and interactions with microbes can have long-lasting physiological impacts on the host. Despite our understanding that early-life microbial interactions are important to host function broadly, the majority of research in this area has been performed in human or model organisms that are not representative of animals in the wild. Specifically, most gut microbiome studies in wildlife are cross-sectional and compare microbial communities across life stages using different individuals, as opposed to tracking the microbial communities and phenotypes of the same individuals from early to later life. This knowledge gap may hinder wildlife microbiome research, as the current model lacks an early-life perspective that can contextualize host phenotypic and fitness differences observed between animals at later life stages. Further, considering early-life microbial dynamics may offer insights to applied research, such as determining the optimal age to manipulate microbiomes for desired conservation outcomes. In this Commentary, we consider current understanding of the importance of early-life host–microbe interactions to vertebrate physiology across the lifespan, discuss why this perspective is necessary in wildlife studies, and provide practical recommendations for experimental designs that can address these questions, including field and laboratory approaches. 

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4. The buzz within: the role of the gut microbiome in honeybee social behavior

   https://doi.org/10.1242/jeb.246400  

   Nguyen, J B; Marshall, C W; Cook, C N (February 2024, Journal of Experimental Biology)

   ABSTRACT Gut symbionts influence the physiology and behavior of their host, but the extent to which these effects scale to social behaviors is an emerging area of research. The use of the western honeybee (Apis mellifera) as a model enables researchers to investigate the gut microbiome and behavior at several levels of social organization. Insight into gut microbial effects at the societal level is critical for our understanding of how involved microbial symbionts are in host biology. In this Commentary, we discuss recent findings in honeybee gut microbiome research and synthesize these with knowledge of the physiology and behavior of other model organisms to hypothesize how host–microbe interactions at the individual level could shape societal dynamics and evolution. 

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5. 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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