Lignocellulose degradation by rumen bacterial communities: New insights from metagenome analyses

Gharechahi, Javad; Vahidi, Mohammad Farhad; Sharifi, Golandam; Ariaeenejad, Shohreh; Ding, Xuezhi; Han, Jianlin; Salekdeh, Ghasem Hosseini

doi:10.1016/j.envres.2023.115925

Cited by 35 publications

(22 citation statements)

References 139 publications

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“…OMVs have also been shown to be produced by chemoautotrophic symbionts that occur in the trophosome of flatworms of the genus Paracatenula, where they play a critical role in provisioning the host with carbohydrates synthesized by the symbionts (Jäckle et al ., 2019). In the human gut microbiome, members of Bacteroides have been shown to tailor OMV content to specific polysaccharides (Sartorio et al ., 2023), and OMVs produced by human and ruminant gut bacteria, including Bacteroides, Fibrobacter, and Clostridium, communally degrade polysaccharides into nutrients available to the hosts (Rakoff-Nahoum et al ., 2014; Arntzen et al ., 2017; Gharechahi et al ., 2023).…”

Section: Discussionmentioning

confidence: 99%

“…Bacteria use a variety of mechanisms to degrade lignocellulosic substrates in their environments. For example, polysaccharide-degrading bacteria, including the common rumen bacteria Bacteroides , Clostridia , and Fibrobacter, use the type IX secretion pathway (T9SS) to secrete large molecular-weight proteins, including multidomain carbohydrate-active enzymes (CAZymes) (Gharechahi et al ., 2023). These enzymes may be released into the environment or bound to the cell envelope (McGavin et al ., 1990; Cai et al ., 1999; Yan and Wu, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Outer membrane vesicles can contribute to cellulose degradation inTeredinibacter turnerae,a cultivable intracellular endosymbiont of shipworms

Gasser,

Liu,

Altamia

et al. 2024

Preprint

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Teredinibacter turnerae is a cultivable cellulolytic Gammaproeteobacterium (Cellvibrionaceae) that commonly occurs as an intracellular endosymbiont in the gills of wood-eating bivalves of the family Teredinidae (shipworms). The genome of T. turnerae encodes a broad range of enzymes that deconstruct cellulose, hemicellulose, and pectin and contribute to lignocellulose digestion in the shipworm gut. However, the mechanism by which symbiont-made enzymes are secreted by T. turnerae and subsequently transported to the site of lignocellulose digestion in the shipworm gut is incompletely understood. Here, we show that T. turnerae cultures grown on carboxymethyl cellulose (CMC) produce outer membrane vesicles (OMVs) that contain a variety of proteins identified by LC-MS/MS as carbohydrate-active enzymes with predicted activities against cellulose, hemicellulose, and pectin. Reducing sugar assays and zymography confirm that these OMVs retain cellulolytic activity, as evidenced by hydrolysis of CMC. Additionally, these OMVs were enriched with TonB-dependent receptors, which are essential to carbohydrate and iron acquisition by free-living bacteria. These observations suggest potential roles for OMVs in lignocellulose utilization by T. turnerae in the free-living state, in enzyme transport and host interaction during symbiotic association, and in commercial applications such as lignocellulosic biomass conversion.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Outer membrane vesicles can contribute to cellulose degradation inTeredinibacter turnerae,a cultivable intracellular endosymbiont of shipworms

Gasser,

Liu,

Altamia

et al. 2024

Preprint

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“…Pectin degradation is carried out by the combined action of two enzymatic classes: methylesterases, which remove the methoxyl groups from pectin with the consequent depolymerization of the demethylated poly-galacturonate, and pectin lyases, which depolymerize pectin. Members of Bacteroidetes and Spirochetes ( Treponema ) were previously identified as the major pectinolytic organisms in host microbiomes [ 51 – 54 ]. In our study, transcripts annotated as PLs were affiliated with Neocallimastigaceae , Oscillospiraceae, Fibrobacteraceae , and Treponemataceae (Fig.…”

Section: Discussionmentioning

confidence: 99%

Structural and functional analysis of the active cow rumen’s microbial community provides a catalogue of genes and microbes participating in the deconstruction of cardoon biomass

Firrincieli,

Minuti,

Cappelletti

et al. 2024

Biotechnol Biofuels

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Background Ruminal microbial communities enriched on lignocellulosic biomass have shown considerable promise for the discovery of microorganisms and enzymes involved in digesting cell wall compounds, a key bottleneck in the development of second-generation biofuels and bioproducts, enabling a circular bioeconomy. Cardoon (Cynara cardunculus) is a promising inedible energy crop for current and future cellulosic biorefineries and the emerging bioenergy and bioproducts industries. The rumen microbiome can be considered an anaerobic “bioreactor”, where the resident microbiota carry out the depolymerization and hydrolysis of plant cell wall polysaccharides (PCWPs) through the catalytic action of fibrolytic enzymes. In this context, the rumen microbiota represents a potential source of microbes and fibrolytic enzymes suitable for biofuel production from feedstocks. In this study, metatranscriptomic and 16S rRNA sequencing were used to profile the microbiome and to investigate the genetic features within the microbial community adherent to the fiber fractions of the rumen content and to the residue of cardoon biomass incubated in the rumen of cannulated cows. Results The metatranscriptome of the cardoon and rumen fibre-adherent microbial communities were dissected in their functional and taxonomic components. From a functional point of view, transcripts involved in the methanogenesis from CO2 and H2, and from methanol were over-represented in the cardoon-adherent microbial community and were affiliated with the Methanobrevibacter and Methanosphaera of the Euryarchaeota phylum. Transcripts encoding glycoside hydrolases (GHs), carbohydrate-binding modules (CBMs), carbohydrate esterases (CEs), polysaccharide lyases (PLs), and glycoside transferases (GTs) accounted for 1.5% (6,957) of the total RNA coding transcripts and were taxonomically affiliated to major rumen fibrolytic microbes, such as Oscillospiraceae, Fibrobacteraceae, Neocallimastigaceae, Prevotellaceae, Lachnospiraceae, and Treponemataceae. The comparison of the expression profile between cardoon and rumen fiber-adherent microbial communities highlighted that specific fibrolytic enzymes were potentially responsible for the breakdown of cardoon PCWPs, which was driven by specific taxa, mainly Ruminococcus, Treponema, and Neocallimastigaceae. Conclusions Analysis of 16S rRNA and metatranscriptomic sequencing data revealed that the cow rumen microbiome harbors a repertoire of new enzymes capable of degrading PCWPs. Our results demonstrate the feasibility of using metatranscriptomics of enriched microbial RNA as a potential approach for accelerating the discovery of novel cellulolytic enzymes that could be harnessed for biotechnology. This research contributes a relevant perspective towards degrading cellulosic biomass and providing an economical route to the production of advanced biofuels and high-value bioproducts.

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“…In the ruminants, maintaining a healthy-balanced microbial community is particularly vital for the reconstruction of rumen and intestinal function, exerting enduring effects on overall health ( 14 – 17 ). These microorganisms possess the capability to generate short-chain fatty acids by breaking down plant polysaccharides such as starch, cellulose, and hemicellulose ( 18 , 19 ). These short-chain fatty acids contribute to thermogenesis and immune function ( 20 , 21 ).…”

Section: Introductionmentioning

confidence: 99%

Crosstalk between innate immunity and rumen-fecal microbiota under the cold stress in goats

Luo,

Zhu,

et al. 2024

Front. Immunol.

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The balance of the microbiome, which is sensitive to temperature changes, plays a crucial role in maintaining overall health and reducing the risk of diseases. However, the specific mechanisms by which immunity and microbiota interact to adapt to cold stress have yet to be addressed. In this study, Nanjiang Yellow goats were chosen as a model and sampled during the cold (winter, cold stress) and warm (spring) seasons, respectively. Analyses of serum immune factors, as well as the composition of rumen and fecal microbial communities, were conducted to explore the crosstalk between microbiota and innate immunity under cold stress. Significantly increased levels of IgA (P < 0.01) were observed in the cold season compared to the warm season. Conversely, the levels of IL-2 (P = 0.02) and IL-6 (P < 0.01) diminished under cold stress. However, no significant differences were observed in IgG (P = 0.89), IgM (P = 0.42), and IL-4 (P = 0.56). While there were no significant changes in the diversity of bacterial communities between the warm and cold seasons, positive correlations between serum IgA, IL-2, IL-6 concentrations and several genera were observed. Furthermore, the weighted gene co-expression network analysis indicated that the microbiota enriched in the MEbrown module positively correlated with IgA, while the microbiota enriched in the MEblue module positively correlated with IL-2 and IL-6. The strong correlation between certain probiotics, including Alistipes, Bacteroides, Blautia, and Prevotellaceae_UCG.004, and the concentration of IL-2, and IL-6 suggests their potential role in immunomodulatory properties. This study provides valuable insights into the crosstalk between microbial communities and immune responses under the challenge of cold stress. Further studies on the immunomodulatory properties of these probiotics would contribute to the development of strategies to enhance the stress resistance of animals for improved overall health and survival.

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Lignocellulose degradation by rumen bacterial communities: New insights from metagenome analyses

Cited by 35 publications

References 139 publications

Outer membrane vesicles can contribute to cellulose degradation inTeredinibacter turnerae,a cultivable intracellular endosymbiont of shipworms

Outer membrane vesicles can contribute to cellulose degradation inTeredinibacter turnerae,a cultivable intracellular endosymbiont of shipworms

Structural and functional analysis of the active cow rumen’s microbial community provides a catalogue of genes and microbes participating in the deconstruction of cardoon biomass

Crosstalk between innate immunity and rumen-fecal microbiota under the cold stress in goats

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