Spatial Structure of the Mormon Cricket Gut Microbiome and its Predicted Contribution to Nutrition and Immune Function

ABSTRACT The human gut microbiome is the subject of intense study due to its importance in health and disease. The majority of these studies have been based on the analysis of feces. However, little is known about how the microbial composition in fecal samples relates to the spatial distribution of microbial taxa along the gastrointestinal tract. By characterizing the microbial content both in intestinal tissue samples and in fecal samples obtained daily, we provide a conceptual framework for how the spatial structure relates to biotic interactions on the community level. We further describe general categories of spatial distribution patterns and identify taxa conforming to these categories. To our knowledge, this is the first study combining spatial and temporal analyses of the human gut microbiome. This type of analysis can be used for identifying candidate probiotics and designing strategies for clinical intervention. The gastrointestinal (GI) microbiome is a densely populated ecosystem where dynamics are determined by interactions between microbial community members, as well as host factors. The spatial organization of this system is thought to be important in human health, yet this aspect of our resident microbiome is still poorly understood. In this study, we report significant spatial structure of the GI microbiota, and we identify general categories of spatial patterning in the distribution of microbial taxa along a healthy human GI tract. We further estimate the biotic interaction structure in the GI microbiota, both through time series and cooccurrence modeling of microbial community data derived from a large number of sequentially collected fecal samples. Comparison of these two approaches showed that species pairs involved in significant negative interactions had strong positive contemporaneous correlations and vice versa, while for species pairs without significant interactions, contemporaneous correlations were distributed around zero. We observed similar patterns when comparing these models to the spatial correlations between taxa identified in the adherent microbiota. This suggests that colocalization of microbial taxon pairs, and thus the spatial organization of the GI microbiota, is driven, at least in part, by direct or indirect biotic interactions. Thus, our study can provide a basis for an ecological interpretation of the biogeography of the human gut. IMPORTANCE The human gut microbiome is the subject of intense study due to its importance in health and disease. The majority of these studies have been based on the analysis of feces. However, little is known about how the microbial composition in fecal samples relates to the spatial distribution of microbial taxa along the gastrointestinal tract. By characterizing the microbial content both in intestinal tissue samples and in fecal samples obtained daily, we provide a conceptual framework for how the spatial structure relates to biotic interactions on the community level. We further describe general categories of spatial distribution patterns and identify taxa conforming to these categories. To our knowledge, this is the first study combining spatial and temporal analyses of the human gut microbiome. This type of analysis can be used for identifying candidate probiotics and designing strategies for clinical intervention. Author Video: An author video summary of this article is available.

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Formula Diet Alters the Ileal Metagenome and Transcriptome at Weaning and during the Postweaning Period in a Porcine Model

mSystems ◽

10.1128/msystems.00457-20 ◽

2020 ◽

Vol 5 (4) ◽

Cited By ~ 1

Author(s):

Ahmed A. Elolimy ◽

Charity Washam ◽

Stephanie Byrum ◽

Celine Chen ◽

Harry Dawson ◽

...

Keyword(s):

Small Intestine ◽

Human Milk ◽

Immune Function ◽

Tight Junctions ◽

Gut Microbiome ◽

Pathogen Detection ◽

Porcine Model ◽

Immune Defense ◽

Milk Formula ◽

The Impact

ABSTRACT Exclusive breastfeeding impacts the intestinal microbiome and is associated with a better immune function than is seen with milk formula (MF) feeding in infants and yet with mechanisms poorly defined. The porcine model was used to evaluate the impact of MF on ileum microbial communities and gene expression relative to human milk (HM)-fed piglets. Fifty-two Dutch Landrace male piglets were fed an isocaloric diet of either HM (n = 26) or MF (n = 26) from day 2 through day 21 of age and weaned to a solid diet until day 51. Eleven piglets from each group were euthanized at day 21, while the remaining piglets (HM, n = 15; MF, n = 15) were euthanized at day 51 to collect ileal epithelium (EP) scrapings and ileal (IL) tissues. The epithelial mucosa was subjected to shotgun metagenome sequencing, and EP and IL tissues were used for transcriptome analysis. On day 21, transcriptome data revealed that the levels of pathways involved in inflammation and apoptosis were significantly higher in MF piglets than in HM piglets, whereas the levels of tight junctions and pathogen detection systems were lower in MF piglets than in HM piglets. The MF impacts on the small intestine were maintained over the postweaning period (day 51) as indicated by higher levels of Dialister invisus bacteria and higher levels of expression of genes associated with inflammation and apoptosis pathways relative to HM group. The current study demonstrated that MF might impact local intestinal inflammation, apoptosis, and tight junctions and might suppress pathogen recognition in the small intestine compared with HM. IMPORTANCE Exclusive human milk (HM) breastfeeding for the first 6 months of age in infants is recommended to improve health outcomes during early life and beyond. When women are unable to provide sufficient HM, milk formula (MF) is often recommended as a complementary or alternative source of nutrition. Previous studies in piglets demonstrated that MF alters the gut microbiome and induces inflammatory cytokine production. The links between MF feeding, gut microbiome, and inflammation status are unclear due to challenges associated with the collection of intestinal samples from human infants. The current report provides the first insight into MF-microbiome-inflammation connections in the small intestine compared with HM feeding using a porcine model. The present results showed that, compared with HM, MF might impact immune function through the induction of ileal inflammation, apoptosis, and tight junction disruptions and likely compromised immune defense against pathogen detection in the small intestine relative to piglets that were fed HM.

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Milk- and solid-feeding practices and daycare attendance are associated with differences in bacterial diversity, predominant communities, and metabolic and immune function of the infant gut microbiome

Frontiers in Cellular and Infection Microbiology ◽

10.3389/fcimb.2015.00003 ◽

2015 ◽

Vol 5 ◽

Cited By ~ 91

Author(s):

Amanda L. Thompson ◽

Andrea Monteagudo-Mera ◽

Maria B. Cadenas ◽

Michelle L. Lampl ◽

M. A. Azcarate-Peril

Keyword(s):

Immune Function ◽

Bacterial Diversity ◽

Gut Microbiome ◽

Feeding Practices ◽

Infant Gut Microbiome

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The Exposome and Immune Health in Times of the COVID-19 Pandemic

Nutrients ◽

10.3390/nu14010024 ◽

2021 ◽

Vol 14 (1) ◽

pp. 24

Author(s):

Javier S. Morales ◽

Pedro L. Valenzuela ◽

Adrián Castillo-García ◽

Javier Butragueño ◽

David Jiménez-Pavón ◽

...

Keyword(s):

Physical Activity ◽

Body Weight ◽

Circadian Rhythms ◽

Immune Function ◽

Weight Management ◽

Gut Microbiome ◽

Potential Role ◽

Sun Exposure ◽

Immune Health

Growing evidence supports the importance of lifestyle and environmental exposures—collectively referred to as the ‘exposome’—for ensuring immune health. In this narrative review, we summarize and discuss the effects of the different exposome components (physical activity, body weight management, diet, sun exposure, stress, sleep and circadian rhythms, pollution, smoking, and gut microbiome) on immune function and inflammation, particularly in the context of the current coronavirus disease 2019 (COVID-19) pandemic. We highlight the potential role of ‘exposome improvements’ in the prevention—or amelioration, once established—of this disease as well as their effect on the response to vaccination. In light of the existing evidence, the promotion of a healthy exposome should be a cornerstone in the prevention and management of the COVID-19 pandemic and other eventual pandemics.

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Structure, culture, and predicted function of the gut microbiome of the Mormon cricketAnabrus simplex(Orthoptera: Tettigoniidae)

10.1101/080846 ◽

2016 ◽

Author(s):

Chad C. Smith ◽

Robert B. Srygley ◽

Frank Healy ◽

Karthikeyan Swaminath ◽

Ulrich G. Mueller

Keyword(s):

Lactic Acid ◽

Community Structure ◽

Lactic Acid Bacteria ◽

16S Rrna ◽

Gut Microbiome ◽

Gene Content ◽

Pathogen Defense ◽

Mormon Cricket ◽

Rrna Sequences ◽

16S Rrna Sequences

SUMMARYThe gut microbiome of insects plays an important role in their ecology and evolution, participating in nutrient acquisition, immunity, and behavior. Microbial community structure within the gut is heavily influenced by differences among gut regions in morphology and physiology, which determine the niches available for microbes to colonize.We present a high-resolution analysis of the structure of the gut microbiome in the Mormon cricketAnabrus simplex,an insect known for its periodic outbreaks in the western United States and nutrition-dependent mating system. The Mormon cricket microbiome was dominated by eleven taxa from the Lactobacillaceae, Enterobacteriaceae, and Streptococcaeae. While most of these were represented in all gut regions, there were marked differences in their relative abundance, with lactic-acid bacteria (Lactobacillaceae) more common in the foregut and midgut and enteric (Enterobacteriaceae) bacteria more common in the hindgut.Differences in community structure were driven by variation in the relative prevalence of three groups: aLactobacillusin the foregut,Pediococcuslactic-acid bacteria in the midgut, andPantoea agglomerans, an enteric bacterium, in the hindgut. These taxa have been shown to have beneficial effects on their hosts in insects and other animals by improving nutrition, increasing resistance to pathogens, and modulating social behavior.Using PICRUSt to predict gene content from our 16S rRNA sequences, we found enzymes that participate in carbohydrate metabolism and pathogen defense in other orthopterans. These were predominately represented in the hindgut and midgut, the most important sites for nutrition and pathogen defense.Phylogenetic analysis of 16S rRNA sequences from cultured isolates indicated low levels of divergence from sequences derived from plants and other insects, suggesting that these bacteria are likely to be exchanged between Mormon crickets and the environment.Our study shows strong spatial variation in microbiome community structure, which influences predicted gene content and thus the potential of the microbiome to influence host function.

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Directional Gaussian Mixture Models of the Gut Microbiome Elucidate Microbial Spatial Structure

mSystems ◽

10.1128/msystems.00817-21 ◽

2021 ◽

Author(s):

Amey P. Pasarkar ◽

Tyler A. Joseph ◽

Itsik Pe’er

Keyword(s):

Spatial Structure ◽

Mixture Models ◽

Gut Microbiome ◽

Gaussian Mixture Models ◽

Experimental Studies ◽

Spatial Arrangement ◽

Gaussian Mixture

The spatial arrangement of the microbes in the gut microbiome is a defining characteristic of its behavior. Various experimental studies have attempted to provide glimpses into the mechanisms that contribute to microbial arrangements.

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Mating promotes lactic-acid gut bacteria in a gift-giving insect

10.1101/071001 ◽

2016 ◽

Author(s):

Chad C Smith ◽

Robert B Srygley ◽

Emma I Dietrich ◽

Ulrich Mueller

Keyword(s):

Lactic Acid ◽

Gut Microbiome ◽

Protein Supplementation ◽

Gut Bacteria ◽

Nuptial Gift ◽

Nuptial Gifts ◽

Beneficial Effects ◽

Host Microbe Interactions ◽

Mormon Cricket ◽

Decorated Cricket

Mating is a ubiquitous social interaction with the potential to influence the microbiome by facilitating transmission, modifying host physiology, and in species where males donate nuptial gifts to females, altering diet. We manipulated mating and nuptial gift consumption in two insects that differ in nuptial gift size, the Mormon cricket Anabrus simplex and the decorated cricket Gryllodes sigillatus, with the expectation that larger gifts are more likely to affect the gut microbiome. Surprisingly, mating, but not nuptial gift consumption, affected bacterial community structure, and only in Mormon crickets. The change in structure was due to a precipitous drop in the abundance of lactic-acid bacteria in unmated females, a taxon known for their beneficial effects on nutrition and immunity. Mating did not affect phenoloxidase or lysozyme-like antibacterial activity in either species, suggesting that any physiological response to mating on host-microbe interactions is decoupled from the systemic immunity. Protein supplementation also did not affect the gut microbiome in decorated crickets, suggesting that insensitivity of gut microbes to dietary protein could contribute to the lack of an effect of nuptial gift consumption. Our study provides experimental evidence that sexual interactions can affect the microbiome and suggests mating can promote beneficial gut bacteria.

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Preservation of three-dimensional spatial structure in the gut microbiome

PLoS ONE ◽

10.1371/journal.pone.0188257 ◽

2017 ◽

Vol 12 (11) ◽

pp. e0188257 ◽

Cited By ~ 8

Author(s):

Yuko Hasegawa ◽

Jessica L. Mark Welch ◽

Blair J. Rossetti ◽

Gary G. Borisy

Keyword(s):

Spatial Structure ◽

Gut Microbiome ◽

Three Dimensional

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The Gut Microbiome as Mediator Between Diet and its Impact on Immune Function

10.21203/rs.3.rs-783504/v1 ◽

2021 ◽

Author(s):

Huiqing Shi ◽

Rob ter Horst ◽

Suzanne Nielen ◽

Mirjam Bloemendaal ◽

Martin Jaeger ◽

...

Keyword(s):

Immune System ◽

Alcohol Consumption ◽

Immune Function ◽

Dietary Patterns ◽

Gut Microbiome ◽

Low Grade ◽

High Alcohol ◽

High Concentrations ◽

Low Grade Inflammation ◽

Prudent Diet

Abstract Background. Dietary habits may influence chronic low-grade inflammation in humans. Here we explore this interaction as well as the potential mediating role of the gut microbiome (GM), given that the GM is both involved in processing of dietary components and influences the immune system. Methods. A cross-sectional analysis of a sample of 482 healthy participants (207 males and 275 females) was performed. Dietary intake was assessed by a semiquantitative food questionnaire. Adipokines and soluble inflammatory mediators were assayed with multiple immunoassays and ELISA. Microbial DNA was extracted from frozen stool samples of the 471 participants. Polychoric correlation analysis was used to establish dietary patterns, and joint multivariate associations between these dietary patterns and immune biomarkers were studied using regression analyses with adjustment for sex, age, BMI, smoking, education levels and physical exercise and other dietary patterns. Non-parametric entropy mediation (NPEM) was applied to investigate whether diet-immune relationships are mediated by abundance of microbial species. Results. We identified 3 dietary patterns, characterized as “high-meat” (meat and sweetened drink), “prudent diet” (fish, fruit, legumes and vegetables) and “high alcohol” (higher alcohol consumption). Higher adherence to prudent diet was associated with a higher adiponectin level. The high alcohol pattern was associated with high concentrations of circulating concentrations of pro-inflammatory markers (CRP, IL-6, VEGF). Dialister invisus was found to mediate the relationship between a prudent dietary pattern and adiponectin, AAT, CRP, IL-6, and VEGF. Conclusion. A meat-based diet and a diet with high alcohol consumption were associated with high concentrations of biomarkers of chronic low-grade inflammation, and conversely, a prudent diet was associated with anti-inflammatory biomarkers. Diet-inflammation regulation may differ between sexes. Mediation analyses revealed that the association between prudent diet and immune function was partially mediated by the GM. Our study adds to our understanding of the associations between diet, the immune system and the GM in a healthy population.

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The Potential Impact of Probiotics on the Gut Microbiome of Athletes

Nutrients ◽

10.3390/nu11102270 ◽

2019 ◽

Vol 11 (10) ◽

pp. 2270 ◽

Cited By ~ 16

Author(s):

Laura Wosinska ◽

Paul D. Cotter ◽

Orla O’Sullivan ◽

Caitriona Guinane

Keyword(s):

Inflammatory Response ◽

Physical Fitness ◽

Immune Function ◽

Gut Microbiome ◽

Athletic Performance ◽

Tissue Repair ◽

Susceptibility To Infection ◽

Potential Impact ◽

And Performance ◽

Exercise Induced

There is accumulating evidence that physical fitness influences the gut microbiome and as a result, promotes health. Indeed, exercise-induced alterations in the gut microbiome can influence health parameters crucial to athletic performance, specifically, immune function, lower susceptibility to infection, inflammatory response and tissue repair. Consequently, maintenance of a healthy gut microbiome is essential for an athlete’s health, training and performance. This review explores the effect of exercise on the microbiome while also investigating the effect of probiotics on various potential consequences associated with over-training in athletes, as well as their associated health benefits.

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