An integrated meta-omics approach reveals substrates involved in synergistic interactions in a bisphenol A (BPA)-degrading microbial community

Abstract

BackgroundUnderstanding microbial interactions in engineering bioprocesses is important to enhance and optimize performance outcomes and requires dissection of the multi-layer complexities of microbial communities. However, unraveling microbial interactions as well as substrates involved in complex microbial communities is a challenging task. Here, we demonstrate an integrated approach of metagenomics, metatranscriptomics, and targeted metabolite analysis to identify the substrates involved in interspecies interactions from a potential cross-feeding model community—bisphenol A (BPA)-biodegrading community, aiming to establish an identification method of microbial interactions in engineering or environmental bioprocesses.ResultsThe community-level BPA-metabolic pathway was constructed using integrated metagenomics and targeted metabolite analyses. The dynamics of active functions and metabolism of major community members were identified using metagenomic and metatranscriptomic analyses in concert. Correlating the community BPA biodegradation performance to the individual bacterial activities enabled the discovery of substrates involved in a synergistic interaction of cross-feeding between BPA-degrading Sphingonomas species and intermediate users, Pseudomonas sp. and Pusillimonas sp. This proposed synergistic interaction was confirmed by the co-culture of a Sphingonomas sp. and Pseudomonas sp. isolates, which demonstrated enhanced BPA biodegradation compared to the isolate of Sphingonomas sp. alone.ConclusionThe three types of integrated meta-omics analyses effectively revealed the metabolic capability at both community-wide and individual bacterial levels. The correlation between these two levels revealed the hidden connection between apparent overall community performance and the contributions of individual community members and their interactions in a BPA-degrading microbial community. In addition, we demonstrated that using integrated multi-omics in conjunction with culture-based confirmation approach is effective to elucidate the microbial interactions affecting the performance outcome. We foresee this approach would contribute the future application and operation of environmental bioprocesses on a knowledge-based control.Electronic supplementary materialThe online version of this article (10.1186/s40168-019-0634-5) contains supplementary material, which is available to authorized users.

Biodegradation of Endocrine Disruptor Bisphenol A by Pseudomonas putida Strain YC-AE1 Isolated from Polluted Soil, Guangdong, China

“…With the degradation time further going on, there was nonsignificant decreasing in TOC to reach finally 82 % at 64 hours incubation. Although, the TOC depletion percentage in our experiment (82 % after 64 hours) by Pseudomonas putida YC-AE1 was closely similar to that reported by Yu et al [52] that used co-culture of sphingomonas sp. (Sph-2) and…”

“…Pseudomonas sp (84% after 72 hours), Surprisingly, our experiment was conducted with 100 mg l -1 compared with 50 mg l -1 BPA by Yu et al [52], and these results reflect the high degradation and mineralization rate of our strain YC-AE1. These results have a good consistency with those reported by Eio et al [53].…”

“…Biodegradation of BPA and its metabolic intermediates could not fully support the mineralization of BPA, TOC experiment could show the mineralization rate of BPA. Although, faster BPA mineralization rate has generally been reported for microbial communities than the culture of BPA-degrading lonely strains [52], interestingly, our strain Pseudomonas putida YC-AE1 lonely demonstrated high BPA mineralization compared with microbial communities. As shown in Fig.…”

Biodegradation of endocrine disruptor Bisphenol A by Pseudomonas putida strain YC-AE1 isolated from polluted soil, Guangdong, China

“…(Sph-2) and Pseudomonas sp. (84% after 72 h), Surprisingly, our experiment was conducted with 100 mg l − 1 compared with 50 mg l − 1 BPA by Yu et al [45], and these results reflect the high degradation and mineralization rate of our strain YC-AE1.…”

“…Biodegradation of BPA and its metabolic intermediates could not fully support the mineralization of BPA, TOC experiment could show the mineralization rate of BPA. Although, faster BPA mineralization rate has generally been reported for microbial communities than the culture of BPA-degrading lonely strains [45], interestingly, our strain Pseudomonas putida YC-AE1 lonely demonstrated high BPA mineralization compared with microbial communities. Although, the TOC depletion percentage in our experiment (82% after 64 h) by Pseudomonas putida YC-AE1 was closely similar to that reported by Yu et al [45] that used co-culture of sphingomonas sp.…”