Healthy gut microbiomes are host-controllable microbiomes

Frontiers in Microbiology, Journal Year: 2025, Volume and Issue: 15

Published: Jan. 8, 2025

Introduction"The instinct of each species is good for itself but has never, as far we can judge, been produced the exclusive others" (1). Why, then, do humans and other mammals benefit from their microbes?Evolutionary theory predicts that natural selection act at organizational levels higher than gene or individual—such on groups even species—provided selective advantages group outweigh evolutionary conflicts. Darwin suggested "on family, not individual," "for sake gaining a serviceable end" This idea was later formalized kin (2). Even distantly related organisms align goals, demonstrated by longstanding partnership between eukaryotic cells mitochondria (3).Microbes are an integral part animal plant hosts, fulfilling essential physiological roles, such enabling access to otherwise unavailable nutrients, training immune system, supporting mucosal development, providing protection. Some microbes vertically transmitted parents offspring. The numerous examples performing vital functions macrobial hosts makes it tempting assume residing within our bodies—particularly in guts—evolved share common interests potential conflicts (4–7). Supporting this assumption, several reports suggest selected harboring "good" these thrive helping example, contributing over 95% organism's genetic repertoire (7–9). But group-level necessary sufficient mechanism explain why microbiomes hosts?Microbes certainly influence host's chances survival reproductive success (10,11) reasons would reduce own fitness form evolutionarily aligned with microbial populations—an condition selection—are easily explained (12,13). For during 25-year human generation, gut undergo more 50,000 generations (assuming conservative four-hour generation time), competing thousands species. Roughly half bacterial biomass colon lost daily replaced new growth (14,15). Before reproduces, any trait unfavorable microbe's likely be eliminated. Moreover, relatively open regularly exposed diverse environmental microbes. Vertical transmission accounts only small fraction microbiome. About twenty consistently shared among most adults (16). How, evolution shaped diverse, rapidly evolving ecosystem individual health?One might argue microbes, host mitigates conflicts, encouraging sacrifice some benefit. However, evolve, genotypes similar needs emerge exploit host-provided without incurring costs—an example tragedy commons (17). These benefits all compatible whether they contribute well-being, creating imbalance contributors free riders. A rider, could bacterium feeds mucin glycans provided while invading tissue potentially causing severe illness.Why, microbes? recent model Sharp & Foster suggests one way overcome conundrum evolve mechanisms actively control limit opportunities evade (18). require enforcement policing maintain cooperation (19). In view, "beneficial" ability healthy state. words, favor microbiome engineers—or, accurately, tinkerers (20)—who make use various methods reach landscape sustain include responses ranging rudimentary inflammation diarrhea sophisticated driven adaptive system. From perspective, theory—the study how systems regulate themselves achieve desired outcomes—parallels host-microbial interactions, suggesting be, definition, host-controllable microbiomes.Will large complex stable?In 1970s, writing Nature, Robert May proposed stability ecosystems complexity increases, particularly number strength interactions grow (21). analyzed simplified Generalized Lotka-Volterra (GLV) explore concept. simulates random communities where population sizes constrained resource availability (represented negative self-interactions) mutual positive influences another's growth. According GLV model, assembled predicted remain stable when sufficiently weak strong confined few (Figure 1). GLV-like models commonly applied microbiomes, stability/complexity trade-offs assumed hold (22,23). May's introducing controller—an agent directs system toward predetermined objective, through energy expenditure—is continuously stabilize unstable reshape stability-complexity Figure 1. Fraction controller 10,000 simulations. Random were simulated increasing interaction strengths numbers Each dot represents hundred simulations colored according resulted Dark blue dots indicate cases 100 unstable, dark red stable. white transition zone intermediate stability. results show adding controller—here idealized device senses microbiome's current composition adjusts rates guide composition—significantly increases range microbiomes. Stability, defined here following original refers returns equilibrium after perturbation based signs eigenvalues Jacobian matrix point. Increased diversity generally associated gut. patients suffering pathogen invasions, inflammation, colitis, inflammatory bowel disease, colorectal cancer reduced alpha compared controls. Similarly, factors aging, obesity, Western diet, urbanization also linked decline (24). Diversity necessarily cause microbiome, rather consequence indirect evidence control. effectively drives state, which, state occur absence (due, constraints). case, impaired, declines. biological systems, active instead diversity. laboratory techniques like media dilution-to-extinction procedures, which isolate single strains, antibiotics, physical barriers, extreme pH, heat conditions similarly nature, see reducing diversity, Hawaiian bobtail squid, isolates Vibrio fischeri ocean its light organ (25). less often appreciated promote greater control.An intriguing underexplored perspective controls declining may signal loss controllability, instance, established reactors simulate gastrointestinal tract significantly stool inocula (26). Although replicate physicochemical flow gut, lack host-control mechanisms, dynamically regulated factors. Overall, viewing interconnected, island-like ecosystem—where serves patch colonized dispersal, local diversification, selection, drift (27)—becomes clearer consider processes active, energy-expending efforts target composition, functions.Beyond extends "state-space," includes populations biochemical activities. ideal scenario tight, full-state control, both abundance function population, including chemical outputs inputs. realistic involves limited, partial-state exerts varying degrees distinct aspects state-space. theoretical framework controlled targeting specific sets referred "minimal elements" (28). achieved leveraging species-species chains connecting external controllers intrinsic dynamics community still lacks empirical validation, highlights identifying elements restore dysbiotic microbiome.How helps microbiomesThe mammalian contains (29,30), categorized into microbiome-independent microbiome-dependent processes. transit time ranges two five hours intestine ten fifty-nine (31). parameters directly microbiome—favoring absorption fermentation intestine—but independent sensing features. open-loop (32)—that is, operate feedback itself. By contrast, system's features exemplifies closed-loop controller, actions dynamics. Evolving allowed fine-tune maximize large, densely populated meta-study comparing cultures fresh samples that, degrees, environment (e.g., SHIME, TIM-2) found interindividual variation inoculum primary driver (33)—i.e., outweighs pressure exerted reactor's operational design (biotope). ensures widely different, personalized communities, lifetime, continue perform despite variability.Controllability observability fundamental controlIf then need experimental elucidate control: (which state-space observe?) controllability states inputs, ideally finite time?). Numerous studies associate high consumption simple sugars low dietary fiber intake underlying debated. One possible explanation observability.Experiments synthetic substrates result history dependence, diverge taxonomic (34–36). lead deterministic compositions, (37). Put simply, multiple grown substrates, isolated same source maintained under identical (35). subset correspond communities. states. tend converge compositions metabolic profiles, regardless sources (37,38). scenario, outside reach. richness respond poorly therapeutic interventions, restriction immunotherapy (39).Controllability inherently dependent observability. Specifically, colonization events educate recognize pathogens enhance monitor Bacteroides fragilis produces immunomodulatory polysaccharide germ-free mice, trains protect against Helicobacter hepaticus, responsible colitis immunocompromised animals (40,41). Another segmented filamentous bacteria (SFB) (Candidatus Arthromitus), species-specific guts vertebrates. SFB forms millimeter-long filaments attach ileal epithelium via specialized cell called holdfast, triggering (42). species, peaks early life (43), future invasive pathogens.Interestingly, occupies spatial gradient cable bacteria, oxygen-rich anoxic lumen. morphology—long, single-layered filaments—it remains tested plays ecological role conducting electrons zones (44) sharing them (45). Ericsson colleagues observed mice exoelectrogenic fuel cells, though electrodes (46). Their showed differences electrical production exoelectrogens predictive lymphocyte trafficking unique signatures locations unusual signatures. adapting response redox gradients, observe react changes state-space.Host-microbiome dynamics: Pinocchio GeppettoOverall, incurs costs host, gathering information acting information. minimize invest reproduction. Over different timescales, arms race develops populations: efficient, cost-effective strategies, ways control—especially restricts (29). systemic counter invasion. When triggered, reactive oxygen released. opportunistic tolerating released hydrogen peroxide expressing molecular machinery allows absorb cytoplasm. There, quickly convert respiratory chain, giving advantage fermentative (47). Salmonella enterica serotype Typhimurium goes step further. Under normal conditions, detoxifies sulfide, quantities microbiota, converting thiosulfate. During thiosulfate tetrathionate, S. respires (48), feeding defense mechanisms.A healthy, symbiotic regulatory ensure beneficial function. arises impaired—whether because becomes unreachable, cues become unobservable, (effectors) ineffective. Geppetto (49); instead, attempt them. Like Pinocchio, strive—and succeed—to

Language: Английский

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Caenorhabditis nematodes influence microbiome and metabolome characteristics of their natural apple substrates over time

mSystems, Journal Year: 2025, Volume and Issue: unknown

Published: Jan. 10, 2025

ABSTRACT The microbiomes of host organisms and their direct source environments are closely linked key for shaping microbial community dynamics. relationship between these dynamics is largely unexplored because substrates usually unavailable. To address this current knowledge gap, we employed bacteriovorous Caenorhabditis nematodes as a unique model system, which like rotting apples can be easily collected. We compared single with corresponding apple substrates, well nematode-free over 2-year sampling period in the botanical garden Kiel, Germany. found that worms have microbiomes, overlap most strongly from same apple. A comparison to previous, related work revealed variation microbiome composition natural isolates significantly influenced by substrate type, were obtained (e.g., fruits or compost). Our further showed assembly mostly driven dispersal limitation. Importantly, two independent analysis approaches consistently suggest worm influence characteristics possibly indicating niche construction nematodes. Moreover, combining metabolome data, identified individual microbes specific compounds indicative fruit ripening associated nematode presence. In conclusion, our study elucidates complex directly connected microbiomes. analyses underscore significant on and, consequently, fruit’s metabolic capacity, thereby enhancing general understanding host–microbiome interactions habitat. IMPORTANCE Almost all community, microbiome. This diverse functions, such food processing, protection against parasites, development. critically depends may shaped environment, process often not understood unavailability substrates. Here, used system facilitates Based period, (i) clear link (ii) (iii) presence sampled Overall, enhances resulting functions.

Language: Английский

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Construction of high-efficiency denitrifying biofilms on hollow fiber membranes through the in situ production and supply of volatile fatty acids

Separation and Purification Technology, Journal Year: 2025, Volume and Issue: unknown, P. 131447 - 131447

Published: Jan. 1, 2025

Language: Английский

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Small molecule metabolites drive plant rhizosphere microbial community assembly patterns

Frontiers in Microbiology, Journal Year: 2025, Volume and Issue: 16

Published: Feb. 11, 2025

The assembly of rhizosphere microbial communities is essential for maintaining plant health, yet it influenced by a wide range biotic and abiotic factors. key drivers shaping the composition these communities, however, remain poorly understood. In this study, we analyzed 108 samples evaluated root traits, growth characteristics, soil enzyme activities, metabolites, chemical properties to identify primary determinants community assembly. Across 36 samples, obtained 969,634 high-quality sequences, clustering into 6,284 ASVs predominantly classified Proteobacteria (57.99%), Actinobacteria (30%), Bacteroidetes (5.13%). Our findings revealed that metabolites accounted more variance in compared (ANOVA, F = 1.53, p 0.04), or traits 1.04, 0.001). Seven small molecule including glycerol, sorbitol, phytol, alpha-ketoglutaric acid, were significantly correlated with βNTI, underscoring their role as critical genus Rhizobium , associated βNTI (R 0.25, 0.009), emerged keystone taxon structure. Soil culture experiments further validated can modulate ST treatment, enriched produced 1,032,205 sequences exhibited significant shifts (Adonis, 0.001, R 0.463), showing higher abundance control (CK). Variable selection (βNTI >2) drove phylogenetic turnover ST, while stochastic processes (|βNTI| < 2) dominated CK. This study provides quantitative insights highlights potential targeted modulation microbiomes.

Language: Английский

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Towards synthetic ecology: strategies for the optimization of microbial community functions

Frontiers in Synthetic Biology, Journal Year: 2025, Volume and Issue: 3

Published: March 18, 2025

Microbial communities are able to carry out myriad functions of biotechnological interest, ranging from the degradation industrial waste synthesis valuable chemical products. Over past years, several strategies have emerged for design microbial and optimization their functions. Here we provide an accessible overview these strategies. We highlight how principles synthetic biology, originally devised engineering individual organisms sub-organismal units (e.g., enzymes), influenced development field ecology. With this, aim encourage readers critically evaluate insights biology should guide our approach community-level engineering.

Language: Английский

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Dysbiosis in the urban tree microbiome

Research Square (Research Square), Journal Year: 2025, Volume and Issue: unknown

Published: March 25, 2025

The tree microbiome is a critical determinant of and ecosystem functioning, but human disturbances can disrupt natural microbe-tree relationships. Here, we show that urban trees exhibit microbial dysbiosis along model urbanization gradient, with declines in mutualistic root leaf symbionts, increases decomposers pathogens, including those relevant to plant, animal, health. These shifts correlate stressors such as heat, drought, atmospheric deposition. Urban microbiomes also altered biogeochemical cycling capabilities, high potential for nitrogen loss through greenhouse gas (N2O) production reduced capacity methane consumption relative rural trees. Additionally, reduces overall diversity, particularly among non-pathogenic microbes, potentially diminishing the ecological health benefits diverse environmental cities. findings underscore need consider forestry management practices maximize city greening forest conservation efforts.

Language: Английский

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miMatch: a microbial metabolic background matching tool for mitigating host confounding in metagenomics research

Gut Microbes, Journal Year: 2024, Volume and Issue: 16(1)

Published: Nov. 27, 2024

Metagenomic research faces a persistent challenge due to the low concordance across studies. While matching host confounders can mitigate impact of individual differences, influence factors such as genetics, environment, and lifestyle habits on microbial profiles makes it exceptionally challenging create fully matched cohorts. The metabolic background, which modulates composition, reflects cumulative confounders, serving an ideal baseline for sample matching. In this study, we introduced miMatch, innovative metagenomic sample-matching tool that uses background comprehensive reference host-related variables employs propensity score build case-control pairs, even in absence confounders. simulated datasets, miMatch effectively eliminated thereby enhancing accuracy identifying differential patterns reducing false positives. Moreover, real data, improved result consistency model generalizability cohorts same disease. A user-friendly web server (https://www.biosino.org/iMAC/mimatch) has been established promote integration multiple cohorts, strengthening causal relationships research.

Language: Английский

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The forgotten wine: Understanding palm wine fermentation and composition

International Journal of Food Microbiology, Journal Year: 2024, Volume and Issue: 429, P. 111022 - 111022

Published: Dec. 12, 2024

Palm wine is an alcoholic beverage that has existed for centuries and important economic socio-culture values in many tropical sub-tropical countries. Lesser known than other types of wines, palm made by spontaneous fermentation sap naturally occurring microbial communities. The ecosystem unique composition diversity, which determines the eventual likely affected geographical distinctiveness. While these features are well understood grape rice wine, have not been wine. Here, we gather information communities metabolite profiles from published studies, covering a wide range methodologies regions to better understand causal links between principal species major metabolites We assessed quality across production local practices provide general characteristics identify specific regional information. These will understandings function contribution variations ensure product this unique, yet overlooked, fermented beverage.

Language: Английский

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Ecological factors affecting toluene biosynthesis from bacterial communities

The Science of The Total Environment, Journal Year: 2024, Volume and Issue: 959, P. 178186 - 178186

Published: Dec. 20, 2024

Language: Английский

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