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

2021 ◽  
Author(s):  
Miaoxiao Wang ◽  
Xiaoli Chen ◽  
xiaonan Liu ◽  
Yuan Fang ◽  
Xin Zheng ◽  
...  

Metabolic division of labor (MDOL) is commonly observed in microbial communities, where a metabolic pathway is sequentially implemented by several members similar to an assembly line. Uncovering the assembly rules of the community engaged in MDOL is crucial for understanding its ecological contribution, as well as for engineering high-performance microbial communities. To investigate the assembly of the community engaged in MDOL, we combined mathematical modelling with experimentations using synthetic microbial consortia. We built a theoretical framework predict the assembly of MDOL system, and derived a simple rule: to maintain co-existence of the MDOL members, the populations responsible for former steps should hold a growth advantage (m) over the "private benefit" (n) of the population responsible for last step, and the steady-state frequency of the last population is determined by the quotient of n and m. Our experiments further indicated that our theoretical framework accurately predicted the stability and assembly of our engineered synthetic consortia that degrade naphthalene through two-step or multi-step MDOL. Our results demonstrate that the assembly of microbial community engaged in MDOL is determined by a limited number of parameters. This quantitative understanding provides novel insights on designing and managing stable microbial systems to address grand challenges facing human society in agriculture, degradation of the environment, and human health.

2005 ◽  
Vol 68 (1) ◽  
pp. 40-48 ◽  
Author(s):  
ANABELLE MATOS ◽  
JAY L. GARLAND

Potential biological control inoculants, Pseudomonas fluorescens 2-79 and microbial communities derived from market sprouts or laboratory-grown alfalfa sprouts, were introduced into alfalfa seeds with and without a Salmonella inoculum. We examined their ability to inhibit the growth of this foodborne pathogen and assess the relative effects of the inoculants on the alfalfa microbial community structure and function. Alfalfa seeds contaminated with a Salmonella cocktail were soaked for 2 h in bacterial suspensions from each inoculant tested. Inoculated alfalfa seeds were grown for 7 days and sampled during days 1, 3, and 7. At each sampling, alfalfa sprouts were sonicated for 7 min to recover microflora from the surface, and the resulting suspensions were diluted and plated on selective and nonselective media. Total bacterial counts were obtained using acridine orange staining, and the percentage culturability was calculated. Phenotypic potential of sprout-associated microbial communities inoculated with biocontrol treatments was assessed using community-level physiological profiles based on patterns of use of 95 separate carbon sources in Biolog plates. Community-level physiological profiles were also determined using oxygen-sensitive fluorophore in BD microtiter plates to examine functional patterns in these communities. No significant differences in total and mesophilic aerobe microbial cell density or microbial richness resulting from the introduction of inoculants on alfalfa seeds with and without Salmonella were observed. P. fluorescens 2-79 exhibited the greatest reduction in the growth of Salmonella early during alfalfa growth (4.22 log at day 1), while the market sprout inoculum had the reverse effect, resulting in a maximum log reduction (5.48) of Salmonella on day 7. Community-level physiological profiles analyses revealed that market sprout communities peaked higher and faster compared with the other inoculants tested. These results suggest that different modes of actions of single versus microbial consortia biocontrol treatments may be involved.


2020 ◽  
Author(s):  
Miaoxiao Wang ◽  
Xiaoli Chen ◽  
Yong Nie ◽  
Xiao-Lei Wu

AbstractMetabolic division of labor (MDOL) is widespread in nature, whereby a complex metabolic pathway is shared between different strains within a community for mutual benefit. However, little is known about how communities engaged in MDOL assemble and spatially organize. We hypothesized that when degradation of an organic compound is carried out via MDOL, substrate concentration and its toxicity modulate the benefit allocation between the two microbial populations, thus governing the assembly of this community. We tested this hypothesis by combining individual-based simulations with pattern formation assays using a synthetic microbial community. We found that while the frequency of the first population increases with an increase in substrate concentration, this increase is capped with an upper bound determined by the biotoxicity of the substrate. In addition, our model showed that substrate concentration and its toxicity affect levels of intermixing between strains. These predictions were quantitatively verified using an engineered system composed of two strains degrading salicylate through MDOL. Our results demonstrate that the structure of the microbial communities can be quantitatively predicted from simple environmental factors, such as substrate concentration and its toxicity, which provides novel perspectives on understanding the assembly of natural communities, as well as insights into how to manage artificial microbial systems.


2020 ◽  
Author(s):  
Huiqin Xie ◽  
Yongli Ku ◽  
Xiangna Yang ◽  
Le Cao ◽  
Xueli Mei ◽  
...  

Abstract Background: Melon (Cucumis melo L.) is one of the most important fruit crops grown in China. However, the yield and quality of melon have significantly declined under continuous cropping. Phenolic acids are believed to be associated with the continuous monocropping obstacle (CMO) and can influence plant microbe interactions. Coumaric acid (CA) is one of the major phenolic acids found in melon root exudates. The objectives of this study were to estimate the elimination of CA by the soil bacterium K3 as well as its effects on mitigating melon CMO. CA degradation was investigated by monitoring the CA retained in the growth medium using high performance liquid chromatography (HPLC). The effects of CA and K3 on rhizosphere soil microbial communities were investigated by the spread plate method and Illumina MiSeq sequencing. Furthermore, the effects of CA and K3 on melon seedling growth were measured under potted conditions. The changes in soil enzymes and fruit quality under K3 amendment were examined in a greenhouse experiment. Result:The results suggest that the addition of CA had the same result as the CMO, such as deterioration of the microbial community and slower growth of melon plants. HPLC and microbial analysis showed that K3 had a pronounced ability to decompose CA and could improve the soil microbial community environment. Soil inoculation with K3 agent could significantly improve the fruit quality of melon.Conclusion: Our results show that the effects of K3 in the soil are reflected by changes in populations and diversity of soil microbes and suggest that deterioration of microbial communities in soil might be associated with the growth constraint of melon in continuous monoculture systems.


2011 ◽  
Vol 77 (21) ◽  
pp. 7560-7567 ◽  
Author(s):  
Marketa Sagova-Mareckova ◽  
Marek Omelka ◽  
Ladislav Cermak ◽  
Zdenek Kamenik ◽  
Jana Olsovska ◽  
...  

ABSTRACTPlant and microbial community composition in connection with soil chemistry determines soil nutrient cycling. The study aimed at demonstrating links between plant and microbial communities and soil chemistry occurring among and within four sites: two pine forests with contrasting soil pH and two grasslands of dissimilar soil chemistry and vegetation. Soil was characterized by C and N content, particle size, and profiles of low-molecular-weight compounds determined by high-performance liquid chromatography (HPLC) of soil extracts. Bacterial and actinobacterial community composition was assessed by terminal restriction fragment length polymorphism (T-RFLP) and cloning followed by sequencing. Abundances of bacteria, fungi, and actinobacteria were determined by quantitative PCR. In addition, a pool of secondary metabolites was estimated byermresistance genes coding for rRNA methyltransferases. The sites were characterized by a stable proportion of C/N within each site, while on a larger scale, the grasslands had a significantly lower C/N ratio than the forests. A Spearman's test showed that soil pH was correlated with bacterial community composition not only among sites but also within each site. Bacterial, actinobacterial, and fungal abundances were related to carbon sources while T-RFLP-assessed microbial community composition was correlated with the chemical environment represented by HPLC profiles. Actinobacteria community composition was the only studied microbial characteristic correlated to all measured factors. It was concluded that the microbial communities of our sites were influenced primarily not only by soil abiotic characteristics but also by dominant litter quality, particularly, by percentage of recalcitrant compounds.


2021 ◽  
Vol 17 (6) ◽  
pp. e1009093
Author(s):  
Pavlos Stephanos Bekiaris ◽  
Steffen Klamt

Microbial communities have become a major research focus due to their importance for biogeochemical cycles, biomedicine and biotechnological applications. While some biotechnological applications, such as anaerobic digestion, make use of naturally arising microbial communities, the rational design of microbial consortia for bio-based production processes has recently gained much interest. One class of synthetic microbial consortia is based on specifically designed strains of one species. A common design principle for these consortia is based on division of labor, where the entire production pathway is divided between the different strains to reduce the metabolic burden caused by product synthesis. We first show that classical division of labor does not automatically reduce the metabolic burden when metabolic flux per biomass is analyzed. We then present ASTHERISC (Algorithmic Search of THERmodynamic advantages in Single-species Communities), a new computational approach for designing multi-strain communities of a single-species with the aim to divide a production pathway between different strains such that the thermodynamic driving force for product synthesis is maximized. ASTHERISC exploits the fact that compartmentalization of segments of a product pathway in different strains can circumvent thermodynamic bottlenecks arising when operation of one reaction requires a metabolite with high and operation of another reaction the same metabolite with low concentration. We implemented the ASTHERISC algorithm in a dedicated program package and applied it on E. coli core and genome-scale models with different settings, for example, regarding number of strains or demanded product yield. These calculations showed that, for each scenario, many target metabolites (products) exist where a multi-strain community can provide a thermodynamic advantage compared to a single strain solution. In some cases, a production with sufficiently high yield is thermodynamically only feasible with a community. In summary, the developed ASTHERISC approach provides a promising new principle for designing microbial communities for the bio-based production of chemicals.


2020 ◽  
Author(s):  
Miaoxiao Wang ◽  
Xiaoli Chen ◽  
Yong Nie ◽  
Xiao-Lei Wu

Abstract Metabolic division of labor (MDOL) is widespread in nature, whereby a complex metabolic pathway is shared between different strains within a community for mutual benefit. However, little is known about how communities engaged in MDOL assemble and spatially organize. We hypothesized that when degradation of an organic compound is carried out via MDOL, substrate concentration and its toxicity modulate the benefit allocation between the two microbial populations, thus governing the assembly of this community. We tested this hypothesis by combining individual-based simulations with pattern formation assays using a synthetic microbial community. We found that while the frequency of the first population increases with an increase in substrate concentration, this increase is capped with an upper bound determined by the biotoxicity of the substrate. In addition, our model showed that substrate concentration and its toxicity affect levels of intermixing between strains. These predictions were quantitatively verified using an engineered system composed of two strains degrading salicylate through MDOL. Our results demonstrate that the structure of the microbial communities can be quantitatively predicted from simple environmental factors, such as substrate concentration and its toxicity, which provides novel perspectives on understanding the assembly of natural communities, as well as insights into how to manage artificial microbial systems.


Author(s):  
Zhang-Xian Xie ◽  
Ke-Qiang Yan ◽  
Ling-Fen Kong ◽  
Ying-Bao Gai ◽  
Tao Jin ◽  
...  

AbstractUnderstanding the mechanisms, structuring microbial communities in oligotrophic ocean surface waters remains a major ecological endeavor. Functional redundancy and metabolic tuning are two mechanisms that have been proposed to shape microbial response to environmental forcing. However, little is known about their roles in the oligotrophic surface ocean due to less integrative characterization of community taxonomy and function. Here, we applied an integrated meta-omics-based approach, from genes to proteins, to investigate the microbial community of the oligotrophic northern Indian Ocean. Insignificant spatial variabilities of both genomic and proteomic compositions indicated a stable microbial community that was dominated by Prochlorococcus, Synechococcus, and SAR11. However, fine tuning of some metabolic functions that are mainly driven by salinity and temperature was observed. Intriguingly, a tuning divergence occurred between metabolic potential and activity in response to different environmental perturbations. Our results indicate that metabolic tuning is an important mechanism for sustaining the stability of microbial communities in oligotrophic oceans. In addition, integrated meta-omics provides a powerful tool to comprehensively understand microbial behavior and function in the ocean.


2018 ◽  
Author(s):  
Laura Gómez-Consarnau ◽  
Rohan Sachdeva ◽  
Scott M. Gifford ◽  
Lynda S. Cutter ◽  
Jed A. Fuhrman ◽  
...  

Aquatic environments contain diverse microbial communities whose complex interactions mediate the cycling of major and trace nutrients such as vitamins. B-vitamins are essential coenzymes that many organisms cannot synthesize. Thus their exchange among de-novo synthesizers and auxotrophs is expected to play an important role in the microbial consortia and explain some of the temporal and spatial changes observed in diversity. In this study, we analyzed metatranscriptomes of a natural coastal microbial community, diel sampled-quarterly over one year to try to identify the potential major B-vitamin synthesizers and consumers. Our transcriptomic data show that the best-represented taxa dominated the expression of synthesis genes for some B-vitamins but lacked transcripts for others. For instance, Rhodobacterales dominated the expression of vitamin-B12synthesis, but not of vitamin-B7, whose synthesis transcripts were mainly represented by Flavobacteria.In contrast, bacterial groups that constituted less than 4% of the community (e.g., Verrucomicrobia) accounted for most of the vitamin-B1synthesis transcripts. Furthermore, ambient vitamin-B1concentrations were higher in samples collected during the day, and were positively correlated with chlorophyll-aconcentration. Our analysis supports the hypothesis that the mosaic of metabolic interdependencies through B-vitamin synthesis and exchange are key processes that contribute to shaping microbial communities in nature.


2021 ◽  
Vol 12 ◽  
Author(s):  
Victor Mataigne ◽  
Nathan Vannier ◽  
Philippe Vandenkoornhuyse ◽  
Stéphane Hacquard

Understanding how microorganism-microorganism interactions shape microbial assemblages is a key to deciphering the evolution of dependencies and co-existence in complex microbiomes. Metabolic dependencies in cross-feeding exist in microbial communities and can at least partially determine microbial community composition. To parry the complexity and experimental limitations caused by the large number of possible interactions, new concepts from systems biology aim to decipher how the components of a system interact with each other. The idea that cross-feeding does impact microbiome assemblages has developed both theoretically and empirically, following a systems biology framework applied to microbial communities, formalized as microbial systems ecology (MSE) and relying on integrated-omics data. This framework merges cellular and community scales and offers new avenues to untangle microbial coexistence primarily by metabolic modeling, one of the main approaches used for mechanistic studies. In this mini-review, we first give a concise explanation of microbial cross-feeding. We then discuss how MSE can enable progress in microbial research. Finally, we provide an overview of a MSE framework mostly based on genome-scale metabolic-network reconstruction that combines top-down and bottom-up approaches to assess the molecular mechanisms of deterministic processes of microbial community assembly that is particularly suitable for use in synthetic biology and microbiome engineering.


mBio ◽  
2012 ◽  
Vol 3 (1) ◽  
Author(s):  
Kristen M. DeAngelis ◽  
Julian L. Fortney ◽  
Sharon Borglin ◽  
Whendee L. Silver ◽  
Blake A. Simmons ◽  
...  

ABSTRACTTropical forest soils decompose litter rapidly with frequent episodes of anoxic conditions, making it likely that bacteria using alternate terminal electron acceptors (TEAs) play a large role in decomposition. This makes these soils useful templates for improving biofuel production. To investigate how TEAs affect decomposition, we cultivated feedstock-adapted consortia (FACs) derived from two tropical forest soils collected from the ends of a rainfall gradient: organic matter-rich tropical cloud forest (CF) soils, which experience sustained low redox, and iron-rich tropical rain forest (RF) soils, which experience rapidly fluctuating redox. Communities were anaerobically passed through three transfers of 10 weeks each with switchgrass as a sole carbon (C) source; FACs were then amended with nitrate, sulfate, or iron oxide. C mineralization and cellulase activities were higher in CF-FACs than in RF-FACs. Pyrosequencing of the small-subunit rRNA revealed members of theFirmicutes,Bacteroidetes, andAlphaproteobacteriaas dominant. RF- and CF-FAC communities were not different in microbial diversity or biomass. The RF-FACs, derived from fluctuating redox soils, were the most responsive to the addition of TEAs, while the CF-FACs were overall more efficient and productive, both on a per-gram switchgrass and a per-cell biomass basis. These results suggest that decomposing microbial communities in fluctuating redox environments are adapted to the presence of a diversity of TEAs and ready to take advantage of them. More importantly, these data highlight the role of local environmental conditions in shaping microbial community function that may be separate from phylogenetic structure.IMPORTANCEAfter multiple transfers, we established microbial consortia derived from two tropical forest soils with different native redox conditions. Communities derived from the rapidly fluctuating redox environment maintained a capacity to use added terminal electron acceptors (TEAs) after multiple transfers, though they were not present during the enrichment. Communities derived from lower-redox soils were not responsive to TEA addition but were much more efficient at switchgrass decomposition. Though the communities were different, diversity was not, and both were dominated by many of the same species of clostridia. This reflects the inadequacy of rRNA for determining the function of microbial communities, in this case the retained ability to utilize TEAs that were not part of the selective growth conditions. More importantly, this suggests that microbial community function is shaped by life history, where environmental factors produce heritable traits through natural selection over time, creating variation in the community, a phenomenon not well documented for microbes.


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