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A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community.

ABSTRACT: Microbial biofilms are omnipresent in nature and relevant to a broad spectrum of industries ranging from bioremediation and food production to biomedical applications. To date little is understood about how multi-species biofilm communities develop and function on a molecular level, due to the complexity of these biological systems. Here we apply a meta-proteomics approach to investigate the mechanisms influencing biofilm formation in a model consortium of four bacterial soil isolates; Stenotrophomonas rhizophila, Xanthomonas retroflexus, Microbacterium oxydans and Paenibacillus amylolyticus. Protein abundances in community and single species biofilms were compared to describe occurring inter-species interactions and the resulting changes in active metabolic pathways. To obtain full taxonomic resolution between closely related species and empower correct protein quantification, we developed a novel pipeline for generating reduced reference proteomes for spectral database searches. Meta-proteomics profiling indicated that community development is dependent on cooperative interactions between community members facilitating cross-feeding on specific amino acids. Opposite regulation patterns of fermentation and nitrogen pathways in Paenibacillus amylolyticus and Xanthomonas retroflexus may, however, indicate that competition for limited resources also affects community development. Overall our results demonstrate the multitude of pathways involved in biofilm formation in mixed communities.

SUBMITTER: Herschend J

PROVIDER: S-EPMC5705676 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community.

Herschend Jakob J Damholt Zacharias B V ZBV Marquard Andrea M AM Svensson Birte B Sørensen Søren J SJ Hägglund Per P Burmølle Mette M

Scientific reports 20171128 1

Microbial biofilms are omnipresent in nature and relevant to a broad spectrum of industries ranging from bioremediation and food production to biomedical applications. To date little is understood about how multi-species biofilm communities develop and function on a molecular level, due to the complexity of these biological systems. Here we apply a meta-proteomics approach to investigate the mechanisms influencing biofilm formation in a model consortium of four bacterial soil isolates; Stenotrop ...[more]

PMID: 29184101

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Project description:BACKGROUND:Understanding 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. RESULTS:The 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. CONCLUSION:The 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.

Project description:We characterized microbial biofilm communities developed over two very closely located but distinct benthic habitats in the Pensacola Bay estuary using two complementary cultivation-independent molecular techniques. Biofilms were grown for 7 days on glass slides held in racks 10 to 15 cm over an oyster reef and an adjacent muddy sand bottom. Total biomass and optical densities of dried biofilms showed dramatic differences for oyster reef versus non-oyster reef biofilms. This study assessed whether the observed spatial variation was reflected in the heterotrophic prokaryotic species composition. Genomic biofilm DNA from both locations was isolated and served as a template to amplify 16S rRNA genes with universal eubacterial primers. Fluorescently labeled PCR products were analyzed by terminal restriction fragment length polymorphism, creating a genetic fingerprint of the composition of the microbial communities. Unlabeled PCR products were cloned in order to construct a clone library of 16S rRNA genes. Amplified ribosomal DNA restriction analysis was used to screen and define ribotypes. Partial sequences from unique ribotypes were compared with existing database entries to identify species and to construct phylogenetic trees representative of community structures. A pronounced difference in species richness and evenness was observed at the two sites. The biofilm community structure from the oyster reef setting had greater evenness and species richness than the one from the muddy sand bottom. The vast majority of the bacteria in the oyster reef biofilm were related to members of the gamma- and delta-subdivisions of Proteobacteria, the Cytophaga-Flavobacterium -Bacteroides cluster, and the phyla Planctomyces and Holophaga-Acidobacterium. The same groups were also present in the biofilm harvested at the muddy sand bottom, with the difference that nearly half of the community consisted of representatives of the Planctomyces phylum. Total species richness was estimated to be 417 for the oyster reef and 60 for the muddy sand bottom, with 10.5% of the total unique species identified being shared between habitats. The results suggest dramatic differences in habitat-specific microbial diversity that have implications for overall microbial diversity within estuaries.

Dataset Information

A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community.

Publications

A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community.

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