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Metagenomic insights into resistant starch degradation by human gut microbiota

ABSTRACT: Metagenomic insights into resistant starch degradation by human gut microbiota

PROVIDER: PRJEB25954 | ENA |

REPOSITORIES: ENA

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			Action	DRS
	ERR2508880_1.fastq.gz	Fastqsanger.gz
	ERR2508880_2.fastq.gz	Fastqsanger.gz
	ERR2508890_1.fastq.gz	Fastqsanger.gz
	ERR2508890_2.fastq.gz	Fastqsanger.gz
	ERR2508900_1.fastq.gz	Fastqsanger.gz

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Project description:Several studies monitoring alterations in the community structure upon resistant starch (RS) interventions are available, although comprehensive function-based analyses are lacking. Recently, a multiomics approach based on 16S rRNA gene sequencing, metaproteomics, and metabolomics on fecal samples from individuals subjected to high and low doses of type 2 RS (RS2; 48 g and 3 g/2,500 kcal, respectively, daily for 2 weeks) in a crossover intervention experiment was performed. In the present study, we did pathway-based metagenomic analyses on samples from a subset of individuals (n = 12) from that study to obtain additional detailed insights into the functional structure at high resolution during RS2 intervention. A mechanistic framework based on obtained results is proposed where primary degradation was governed by Firmicutes, with Ruminococcus bromii as a major taxon involved, providing fermentation substrates and increased acetate concentrations for the growth of various major butyrate producers exhibiting the enzyme butyryl-coenzyme A (CoA):acetate CoA-transferase. H2-scavenging sulfite reducers and acetogens concurrently increased. Individual responses of gut microbiota were noted, where seven of the 12 participants displayed all features of the outlined pattern, whereas four individuals showed mixed behavior and one subject was unresponsive. Intervention order did not affect the outcome, emphasizing a constant substrate supply for maintaining specific functional communities.IMPORTANCE Manipulation of gut microbiota is increasingly recognized as a promising approach to reduce various noncommunicable diseases, such as obesity and type 2 diabetes. Specific dietary supplements, including resistant starches (RS), are often a focus, yet comprehensive insights into functional responses of microbiota are largely lacking. Furthermore, unresponsiveness in certain individuals is poorly understood. Our data indicate that distinct parts of microbiota work jointly to degrade RS and successively form health-promoting fermentation end products. It highlights the need to consider both primary degraders and specific more-downstream-acting bacterial groups in order to achieve desired intervention outcomes. The gained insights will assist the design of personalized treatment strategies based on an individual's microbiota.

Project description:Background Lytic polysaccharide monooxygenases (LPMOs) are often studied in simple models involving activity measurements of a single LPMO or a blend thereof with hydrolytic enzymes towards an insoluble substrate. However, the contribution of LPMOs to polysaccharide breakdown in complex cocktails of hydrolytic and oxidative enzymes, similar to fungal secretomes, remains elusive. Typically, two starch-specific AA13 LPMOs are encoded by mainly Ascomycota genomes. Here, we investigate the impact of LPMO loss on the growth and degradation of starches of varying resistance to amylolytic hydrolases by Aspergillus nidulans. Results Deletion of the genes encoding AnAA13A that possesses a CBM20 starch-binding module, AnAA13B (lacking a CBM20) or both AA13s genes resulted in reduction in growth on solid media with resistant, but not soluble processed potato starch. Larger size and amount of residual starch granules were observed for the AA13 KO strains as compared to the reference and the impairment of granular starch degradation was more severe for the AnAA13A KO based on a microscopic analysis. After five days of growth on raw potato starch in liquid media, the mount of residual starch was about 5-fold higher for the AA13 KO strains compared to the reference, which underscores the importance of LPMOs for degradation of especially resistant starches. Proteomic analyses revealed substantial changes in the secretomes of the AA13 double KO, followed by the AnAA13A deficient strains, whereas no significant changes in the proteome were observed for the AnAA13B deficient strain. Conclusions This study shows that the loss of AA13, especially the starch-binding AnAA13A, impairs degradation of resistant potato starch, but has limited impact less-resistant wheat starch and has no impact at all on processed solubilised starch. The effects of LPMO loss are more pronounced at the later stages of fungal growth, when the less-accessible regions of the substrate accumulate. The striking impact of the loss of a single LPMO against a whole secretome offers insight into the crucial role played by AA13 in the degradation of resistant starch and presents a methodological framework to analyse the contribution of distinct LPMOs towards complex substrates under in vivo conditions.

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Metagenomic insights into resistant starch degradation by human gut microbiota

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