Selfishness driving reductive evolution shapes interdependent patterns in spatially structured microbial communities

Fang, Yuan; Liu, Xiaonan; Nie, Yong; Wu, Xiao‐Lei

doi:10.1038/s41396-020-00858-x

Cited by 35 publications

(39 citation statements)

References 49 publications

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“…Nevertheless, our study also found that predictive function derived from the individual-based (IB) model with the assumption of mass well-mixing was not completely identical to the function from our ordinary differential equation (ODE) model, suggesting that other physical features of spatially structured environment may also contribute to the assembly of MDOL community. For example, the spatial distributions of different cell types in the colony are thought to represent another vital factor that governs community assembly [27, 56–58]. In agreement with previous studies [31, 38, 59], our IB simulations suggested that when two populations engaged in MDOL, cells from the two populations are spatially more proximal to each other than the scenario when the two populations did not exhibit defined interactions (Supplementary Figure 27).…”

Section: Discussionsupporting

confidence: 89%

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Substrate traits shape the structure of microbial community engaged in metabolic division of labor

Fang

Chen

Tang

et al. 2020

Preprint

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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.

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Section: Discussionsupporting

confidence: 89%

“…Here, in our study, we proved that this is also the case in the community engaged in MDOL. In addition, we reconfirmed that limited mass diffusion is one possible way to privatize public benefit [30, 37, 56]. On the one hand, it helps the Embezzler population to privatize the final product for its own growth.…”

Section: Discussionmentioning

confidence: 69%

Substrate traits shape the structure of microbial community engaged in metabolic division of labor

Fang

Chen

Tang

et al. 2020

Preprint

Self Cite

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“…To simulate the spatial competition between two populations, the BacGo model was built based on 2D lattices, following our previous framework(DK 1998; Kreft et al 1998;Wang et al 2020). In our model, a microhabitat was conceptualized as a 20×20 array.…”

Section: Basic Settings Of the Bacgo Modelmentioning

confidence: 99%

“…Abiotic spatially related factors may also be potential factors independent of biological intrinsic properties but affecting outcomes of the competition for space. Our previous study indicated that even if the initial abundance and inherent fitness of two populations were identical, outcomes of the spatial competition were not completely random but significantly influenced by the relative positions and time orders for the emergence of different genotypes (Wang et al 2020). These findings suggested that specific events that occurred during the space colonization affected which population colonized more space.…”

Section: Introductionmentioning

confidence: 99%

Successful microbial colonization of space using an anti-aggregation strategy

Liu

Fang

Nie

et al. 2021

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Many organisms live in habitats with limited nutrients or space, competition for these resources is ubiquitous. Although spatial factors related to population’s manner of colonizing space influences its success in spatial competition, what these factors are and to what extent they influence the outcome remains under-explored. Here, we applied a simulated competitive model to explore the spatial factors affecting outcomes of competition for space. By quantifying spatial factors using ‘Space Accessibility’, we show that colonizing space in an anti-aggregation manner contributes to microbial competitive success. We also find that the competitive edge derived from being anti-aggregation in colonizing space, which results in a higher ‘Space Accessibility’, neutralizes the disadvantage arising from either lower growth rate or lower initial abundance. These findings shed light on the role of space colonization manners on maintaining biodiversity within ecosystems and provide novel insights critical for understanding how competition for space drives evolutionary innovation.

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“…S9 and Table S8). According to the Black Queen Hypothesis, when an individual loses an energy-expensive function, it becomes a 'beneficiary', who scavenges the public goods, such as AAs, from other individuals (helpers) for survival [65,66]. The 'beneficiary' strain will expand in the community until the production of public goods, such as AAs, is just sufficient to support the balanced community.…”

Section: Biosynthetic Metabolism Of Acetate Oxidizersmentioning

confidence: 99%

Chasing the metabolism of novel syntrophic acetate-oxidizing bacteria in thermophilic methanogenic chemostats

Zeng¹,

Zheng

M³

et al. 2021

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Background: Acetate is the major intermediate of anaerobic digestion of organic waste to CH4. In anaerobic methanogenic systems, acetate degradation is carried out by either acetoclastic methanogenesis or a syntrophic degradation by a syntrophy of acetate oxidizers and hydrogenotrophic methanogens. Due to challenges in isolation of syntrophic acetate-oxidizing bacteria (SAOB), the diversity and metabolism of SAOB, as well as the mechanisms of their interactions with methanogenic partners remain poorly understood. Results: In this study, we successfully enriched previously unknown SAOB by operating continuous thermophilic anaerobic chemostats fed with acetate, propionate, butyrate, or isovalerate as the sole carbon and energy source. They represent novel clades belonging to Clostridia, Thermoanaerobacteraceae, Anaerolineae, and Gemmatimonadetes. In these SAOB, acetate is degraded through reverse Wood-Ljungdahl pathway or an alternative pathway mediated by the glycine cleavage system, while the SAOB possessing the latter pathway dominated the bacterial community. Moreover, H2 is the major product of the acetate degradation by these SAOB, which is mediated by [FeFe]-type electron-confurcating hydrogenases, formate dehydrogenases, and NADPH reoxidation complexes. We also identified the methanogen partner of these SAOB in acetate-fed chemostat, Methanosarcina thermophila, which highly expressed genes for CO2-reducing methanogenesis and hydrogenases to supportively consuming H2 at transcriptional level. Finally, our bioinformatical analyses further suggested that these previously unknown syntrophic lineages were prevalent and might play critical roles in thermophilic methanogenic reactors. Conclusion: This study expands our understanding on the phylogenetic diversity and in situ biological functions of uncultured syntrophic acetate degraders, and presents novel insights on how they interact with their methanogens partner. These knowledges strengthen our awareness on the important role of SAO in thermophilic methanogenesis and may be applied to manage microbial community to improve the performance and efficiency of anaerobic digestion. Keywords: Thermophilic anaerobic digestion, Microbial community, Syntrophic acetate oxidation, Glycine cleavage, Energy conservation

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Selfishness driving reductive evolution shapes interdependent patterns in spatially structured microbial communities

Cited by 35 publications

References 49 publications

Substrate traits shape the structure of microbial community engaged in metabolic division of labor

Substrate traits shape the structure of microbial community engaged in metabolic division of labor

Successful microbial colonization of space using an anti-aggregation strategy

Chasing the metabolism of novel syntrophic acetate-oxidizing bacteria in thermophilic methanogenic chemostats

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