Even allocation of benefits stabilizes microbial community engaged in metabolic division of labor

Fang, Yuan; Chen, Xiaoli; Liu, Xiaonan; Yuan, Fang; Zheng, Xin; Huang, Ting; Tang, Yue‐Qin; Ackermann, Martin; Nie, Yong; Wu, Xiao‐Lei

doi:10.1016/j.celrep.2022.111410

Cited by 34 publications

(37 citation statements)

References 83 publications

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“…The underlying mechanism is different resources consumers can affect microbial beneficial distribution (metabolic flux) in microbial ecosystems with metabolic division of labour. The benefits distribution of microbial members is essential to metabolic stability [67]. Our short-term fermentation results demonstrated that batches with stable overexpression of bacterial metabolic genes (longer maintenance of stable beneficial distribution) showed superior temporal metabolic functional stability.…”

Section: Discussionmentioning

confidence: 72%

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

Tan

Zhu

Wijffels

et al. 2023

Preprint

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Background Regulating microbial metabolic stability is an ever-challenging goal in the food industry to ensure the productivity and quality of fermented foods. The microbiome underlying traditional Chinese liquor fermentation is such a representative microbiome metabolism that is affected by many dynamic abiotic/biotic factors. The complex microbial activities bring beneficial qualities (complex and rich aroma profiles, etc.) to the fermented product, but can also cause unstable fermentation outcomes. Here, we designed a three-step experiment (abiotic regulation; biotic regulation; lab-scale validation) to explore which factors cause unstable fermentation outcomes and how to regulate microbiome metabolic functional stability accordingly. Results We found that 30.5% industrial fermentation of traditional Chinese liquor outcomes could be precisely predicted by initial abiotic factors. We could ensure the stability of partial fermentation batches by regulating the initial ratio of acidity to reducing sugar, moisture, and starch. Furthermore, in two representative unpredictable fermentation batches (named batch A and batch B), we found that unstable fermentation outcomes occurred even with similar initial abiotic factors after a dynamic three-phase fermentation. Unstable fermentation batches showed fluctuations in microbial community assembly that affected fermentation stability by altering the beneficial distribution (metabolic flux) of redundant metabolic pathways between yeasts and Lactobacilli. The metabolism of batch B was more stable than that of batch A due to the consistent overexpression of a specific set of bacterial metabolic genes. In repeated feed-batch fermentation processes, the difference in metabolic functional stability between the two batches was amplified 9.02 times. Batch B had significantly lower microbiome metabolic fluctuations than batch A, with higher robustness and lower complexity of the metabolic functional network. Moreover, we found that adjusting the initial microbial inoculation ratio could regulate both the metabolic beneficial distribution and temporal metabolic fluctuations of the microbiome to appropriately reduce the instability caused by biotic factors. Conclusions This study demonstrates that rationally regulating initial parameters and microbial inoculation ratio is a practical strategy to optimize indigenous liquor fermentation. The stable microbial beneficial distribution and high metabolic robustness are essential to obtain the ideal microbiome metabolic stability. Our study provides insights and shows the feasibility of enhancing metabolic functional stability through initial conditions in dynamic microbial ecosystems.

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Section: Discussionmentioning

confidence: 72%

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

Tan

Zhu

Wijffels

et al. 2023

Preprint

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“…We think that research on selection mechanisms may represent the most productive intersection of mathematical modeling with microbial experimental technology. Mathematical models of nearest spatiotemporal niches and metabolic divisions of labor have been constructed and established recently (Wang, Chen, et al, 2022;Zhao et al, 2021), providing new perspectives for quantifying and predicting biotic and abiotic selection.…”

Section: Selectionmentioning

confidence: 99%

Non‐gene‐editing microbiome engineering of spontaneous food fermentation microbiota—Limitation control, design control, and integration

Chen

Wang²,

Teng³

et al. 2023

Comp Rev Food Sci Food Safe

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Non-gene-editing microbiome engineering (NgeME) is the rational design and control of natural microbial consortia to perform desired functions. Traditional NgeME approaches use selected environmental variables to force natural microbial consortia to perform the desired functions. Spontaneous food fermentation, the oldest kind of traditional NgeME, transforms foods into various fermented products using natural microbial networks. In traditional NgeME, spontaneous food fermentation microbiotas (SFFMs) are typically formed and controlled manually by the establishment of limiting factors in small batches with little mechanization. However, limitation control generally leads to trade-offs between efficiency and the quality of fermentation. Modern NgeME approaches based on synthetic microbial ecology have been developed using designed microbial communities to explore assembly mechanisms and target functional enhancement of SFFMs. This has greatly improved our understanding of microbiota control, but such approaches still have shortcomings compared to traditional NgeME. Here, we comprehensively describe research on mechanisms and control strategies for SFFMs based on traditional and modern NgeME. We discuss the ecological and engineering principles of the two approaches to enhance the understanding of how best to control SFFM. We also review recent applied and theoretical research on modern NgeME and propose an integrated in vitro synthetic microbiota model to bridge gaps between limitation control and design control for SFFM.

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“…(2) Engineer a stable MDOL community with a defined structure [8,53] Model derived Metabolic burden; transfer efficiency An MDOL community outperforms a single population only when the benefit derived from reduced metabolic burden overcomes the inefficiency of intermediate transport [54] Engineered strains Parameters involved in a metabolic pathway To maintain the stability of an MDOL community, the populations responsible for the initial steps in a linear metabolic pathway should hold a growth advantage (m) over the "private benefit" (n) of the population responsible for the last step. The steady-state frequency of the last population is then determined by the quotient of n and m [33] Engineered strains Substrate concentration and toxicity The proportion of the population executing the first metabolic step in an MDOL community can be estimated by Monod-like formulas governed by substrate concentration and toxicity [55] synthetic consortia with predefined interaction modes to avoid such unpredictable effects. This type of design can be achieved by engineering the metabolism of the member strains or mimicking cell-cell communications through the construction of genetic circuits, usually based on quorumsensing signals.…”

Section: Pairwise Interactionsmentioning

confidence: 99%

“…This system can be simplified by imposing reasonable assumptions. For example, principles governing the function 54 and assembly 33 of microbial communities engaged in MDOL can be derived from the simplified LVMM model. The genome-scale metabolic model (GSMM) is another useful model for predicting community properties.…”

Section: Mathematical Models In Microbiome Engineeringmentioning

confidence: 99%

“…Controlling the growth of different members could maintain their coexistence and stabilize the community [33][34][35] Engineered strains Cooperative interdependence Cooperative interdependence contributes to the maintenance of the long-term coexistence of multiple species [36] Natural strains Temperature Higher temperatures favor slower-growing bacterial species in multispecies communities…”

Section: Growth Ratementioning

confidence: 99%

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Guided by the principles of microbiome engineering: Accomplishments and perspectives for environmental use

Fang

Huang

et al. 2022

mLife

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Although the accomplishments of microbiome engineering highlight its significance for the targeted manipulation of microbial communities, knowledge and technical gaps still limit the applications of microbiome engineering in biotechnology, especially for environmental use. Addressing the environmental challenges of refractory pollutants and fluctuating environmental conditions requires an adequate understanding of the theoretical achievements and practical applications of microbiome engineering. Here, we review recent cutting-edge studies on microbiome engineering strategies and their classical applications in bioremediation. Moreover, a framework is summarized for combining both top-down and bottom-up approaches in microbiome engineering toward improved applications. A strategy to engineer microbiomes for environmental use, which avoids the build-up of toxic intermediates that pose a risk to human health, is suggested. We anticipate that the highlighted framework and strategy will be beneficial for engineering microbiomes to address difficult environmental challenges such as degrading multiple refractory pollutants and sustain the performance of engineered microbiomes in situ with indigenous microorganisms under fluctuating conditions.

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Even allocation of benefits stabilizes microbial community engaged in metabolic division of labor

Cited by 34 publications

References 83 publications

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

Regulating microbiome metabolic stability for stable indigenous liquor fermentation

Non‐gene‐editing microbiome engineering of spontaneous food fermentation microbiota—Limitation control, design control, and integration

Guided by the principles of microbiome engineering: Accomplishments and perspectives for environmental use

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