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Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem.

ABSTRACT: Because of their agricultural value, there is a great body of research dedicated to understanding the microorganisms responsible for rumen carbon degradation. However, we lack a holistic view of the microbial food web responsible for carbon processing in this ecosystem. Here, we sampled rumen-fistulated moose, allowing access to rumen microbial communities actively degrading woody plant biomass in real time. We resolved 1,193 viral contigs and 77 unique, near-complete microbial metagenome-assembled genomes, many of which lacked previous metabolic insights. Plant-derived metabolites were measured with NMR and carbohydrate microarrays to quantify the carbon nutrient landscape. Network analyses directly linked measured metabolites to expressed proteins from these unique metagenome-assembled genomes, revealing a genome-resolved three-tiered carbohydrate-fuelled trophic system. This provided a glimpse into microbial specialization into functional guilds defined by specific metabolites. To validate our proteomic inferences, the catalytic activity of a polysaccharide utilization locus from a highly connected metabolic hub genome was confirmed using heterologous gene expression. Viral detected proteins and linkages to microbial hosts demonstrated that phage are active controllers of rumen ecosystem function. Our findings elucidate the microbial and viral members, as well as their metabolic interdependencies, that support in situ carbon degradation in the rumen ecosystem.

SUBMITTER: Solden LM

PROVIDER: S-EPMC6784887 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem.

Solden Lindsey M LM Naas Adrian E AE Roux Simon S Daly Rebecca A RA Collins William B WB Nicora Carrie D CD Purvine Sam O SO Hoyt David W DW Schückel Julia J Jørgensen Bodil B Willats William W Spalinger Donald E DE Firkins Jeffrey L JL Lipton Mary S MS Sullivan Matthew B MB Pope Phillip B PB Wrighton Kelly C KC

Nature microbiology 20181024 11

Because of their agricultural value, there is a great body of research dedicated to understanding the microorganisms responsible for rumen carbon degradation. However, we lack a holistic view of the microbial food web responsible for carbon processing in this ecosystem. Here, we sampled rumen-fistulated moose, allowing access to rumen microbial communities actively degrading woody plant biomass in real time. We resolved 1,193 viral contigs and 77 unique, near-complete microbial metagenome-assemb ...[more]

PMID: 30356154

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Project description:BackgroundThe rumen is an ecosystem with a complex microbial microflora in which microbes initiate biofilm formation by attaching to plant surfaces for plant degradation and are capable of converting feed to nutrients and energy via microbial processes. Quorum sensing (QS) is a cell-to-cell communication mechanism that allows microbes to synchronize the expression of multiple genes in the group to perform social behaviors such as chemotaxis and biofilm formation using self-synthesized QS signaling molecules. Whereas QS has been extensively studied in model microorganisms under pure culture conditions, QS mechanisms are poorly understood in complex bacterial communities, such as the rumen microflora, in which cell-to-cell communication may be common.ResultsHere, we analyzed 981 rumens bacterial and archaeal genomes from the Joint Genome Institute (JGI) and GenBank databases and identified 15 types of known QS signaling molecule-related genes. The analysis of the prevalence and abundance of genes involved in QS showed that 767 microbial genomes appeared to possess QS-related genes, including 680 bacterial genomes containing autoinducer-2 (AI-2) synthase- or receptor-encoding genes. Prevotella, Butyivibrio, Ruminococcus, Oribacterium, Selenomonas, and Treponema, known abundant bacterial genera in the rumen, possessed the greatest numbers of AI-2-related genes; these genes were highly expressed within the metatranscriptome dataset, suggesting that intra- and interspecies communication mediated by AI-2 among rumen microbes was universal in the rumen. The QS processes mediated by the dCache_1-containing AI-2 receptors (CahRs) with various functional modules may be essential for degrading plants, digesting food, and providing energy and nutrients to the host. Additionally, a universal natural network based on QS revealed how rumen microbes coordinate social behaviors via the AI-2-mediated QS system, most of which may potentially function via AI-2 binding to the extracellular sensor dCache_1 domain to activate corresponding receptors involved in different signal transduction pathways, such as methyl-accepting chemotaxis proteins, histidine kinases, serine phosphatases, c-di-GMP synthases and phosphodiesterases, and serine/threonine kinases in the rumen.ConclusionsThe exploration of AI-2-related genes, especially CahR-type AI-2 receptors, greatly increased our insight into AI-2 as a potentially "universal" signal mediating social behaviors and will help us better understand microbial communication networks and the function of QS in plant-microbe interactions in complex microecosystems. Video Abstract.

Project description:The purpose of this study was to examine the effects of two pasture feeding systems-perennial ryegrass (GRS) and perennial ryegrass and white clover (CLV)-and an indoor total mixed ration (TMR) system on the (a) rumen microbiome; (b) rumen fluid and milk metabolome; and (c) to assess the potential to distinguish milk from different feeding systems by their respective metabolomes. Rumen fluid was collected from nine rumen cannulated cows under the different feeding systems in early, mid and late lactation, and raw milk samples were collected from ten non-cannulated cows in mid-lactation from each of the feeding systems. The microbiota present in rumen liquid and solid portions were analysed using 16S rRNA gene sequencing, while ¹H-NMR untargeted metabolomic analysis was performed on rumen fluid and raw milk samples. The rumen microbiota composition was not found to be significantly altered by any feeding system in this study, likely as a result of a shortened adaptation period (two weeks' exposure time). In contrast, feeding system had a significant effect on both the rumen and milk metabolome. Increased concentrations of volatile fatty acids including acetic acid, an important source of energy for the cow, were detected in the rumen of TMR and CLV-fed cows. Pasture feeding resulted in significantly higher concentrations of isoacids in the rumen. The ruminal fluids of both CLV and GRS-fed cows were found to have increased concentrations of p-cresol, a product of microbiome metabolism. CLV feeding resulted in increased rumen concentrations of formate, a substrate compound for methanogenesis. The TMR feeding resulted in significantly higher rumen choline content, which contributes to animal health and milk production, and succinate, a product of carbohydrate metabolism. Milk and rumen-fluids were shown to have varying levels of dimethyl sulfone in each feeding system, which was found to be an important compound for distinguishing between the diets. CLV feeding resulted in increased concentrations of milk urea. Milk from pasture-based feeding systems was shown to have significantly higher concentrations of hippuric acid, a potential biomarker of pasture-derived milk. This study has demonstrated that ¹H-NMR metabolomics coupled with multivariate analysis is capable of distinguishing both rumen-fluid and milk derived from cows on different feeding systems, specifically between indoor TMR and pasture-based diets used in this study.

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Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem.

Publications

Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem.

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