Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Xiao, Kangpeng; Liang, Xianghui; Lu, Haoran; Li, Xiaobing; Zhang, Zhipeng; Lu, Xingbang; Wang, Hai; Meng, Yafei; Roy, Ayan; Luo, Wen; Shen, Xuejuan; Irwin, David M.; Shen, Yongyi

doi:10.1038/s41396-022-01247-2

Cited by 25 publications

(13 citation statements)

References 90 publications

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“…Notably, elevated microbiota alpha diversity (richness and evenness) and the number of KOs were detected with increased intake of plant fiber, possibly mirroring a need for more diverse microbial populations for a hard-to-digest diet 21 , 22 . This result was expected since the transformation of complex substrates into end products is typically accomplished through a number of metabolic stages mediated by inter-connected microbial groups 23 – 25 .…”

Section: Discussionmentioning

confidence: 89%

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons

Fei

Luo

et al. 2023

npj Biofilms Microbiomes

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Wild animals may encounter multiple challenges especially food shortage and altered diet composition in their suboptimal ranges. Yet, how the gut microbiome responds to dietary changes remains poorly understood. Prior studies on wild animal microbiomes have typically leaned upon relatively coarse dietary records and individually unresolved fecal samples. Here, we conducted a longitudinal study integrating 514 time-series individually recognized fecal samples with parallel fine-grained dietary data from two Skywalker hoolock gibbon (Hoolock tianxing) groups populating high-altitude mountainous forests in western Yunnan Province, China. 16S rRNA gene amplicon sequencing showed a remarkable seasonal fluctuation in the gibbons’ gut microbial community structure both across individuals and between the social groups, especially driven by the relative abundances of Lanchnospiraceae and Oscillospiraceae associated with fluctuating consumption of leaf. Metagenomic functional profiling revealed that diverse metabolisms associated with cellulose degradation and short-chain fatty acids (SCFAs) production were enriched in the high-leaf periods possibly to compensate for energy intake. Genome-resolved metagenomics further enabled the resolving metabolic capacities associated with carbohydrate breakdown among community members which exhibited a high degree of functional redundancy. Our results highlight a taxonomically and functionally sensitive gut microbiome actively responding to the seasonally shifting diet, facilitating the survival and reproduction of the endangered gibbon species in their suboptimal habitats.

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Section: Discussionmentioning

confidence: 89%

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons

Fei

Luo

et al. 2023

npj Biofilms Microbiomes

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“…The gut microbes involved in lignin breakdown have only been characterized in animals that have evolutionarily adapted to feed on a lignocellulose diet. [52,53] Here, we further explored the potential interrelationships between the genus-level bacterial groups and lignin metabolism in rats using RDA. The RDA displays the variation explained in the gut microbiota (50.4%), constrained by the results from pyr-GC/MS, that is, both Sand G-type lignin, their sum and ratio (Figure 6).…”

Section: The Association Of Lignin Content Composition and Metabolite...mentioning

confidence: 99%

Metabolic Fate of Lignin in Birch Glucuronoxylan Extracts as Dietary Fiber Studied in a Rat Model

Lahtinen,

Kynkäänniemi,

Jian

et al. 2023

Molecular Nutrition Food Res

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ScopeWhile previously considered inert, recent studies suggest lignin metabolism with unknown metabolic fates is occurring in the gastrointestinal tract of several animal models. This study focuses on analyzing the potential metabolites of lignin.Methods and resultsThe diets of rats include relatively pure birch glucuronoxylan (pureGX) with residual lignin or lignin‐rich GX (GXpoly) in their diet. Nuclear magnetic spectroscopy of the lignin isolated from the GXpoly‐fed rats fecal sample shows high alteration in chemical structure, whereas lignin‐carbohydrate complexes (LCCs) are enriched in fecal samples from the pureGX group. Moreover, the increased syringyl‐to‐guaiacyl (S/G) ratio suggests that lignin G‐units are predominantly metabolized based on pyrolysis gas chromatography–mass spectrometry (pyr‐GC/MS). The presence of small phenolic metabolites identified in urine samples of the GXpoly group, for example, ferulic and sinapic acids, their sulfate and glucuronide derivatives, and 4‐sulfobenzylalcohol, suggests that the small fragmented lignin metabolites in the large intestine enter the plasma, and are further processed in the liver. Finally, the relative abundances of polyphenol‐degrading Enterorhabdus and Akkermansia in the gut microbiota are associated with lignin metabolism.ConclusionThese findings give further evidence to lignin metabolism in the gut of nonruminants and provide insight to the potential microbes and metabolic routes.

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“…The spalacid filovirus-like elements also have RNA expression products. For example, searching a transcriptome project in bamboo rats (R. pruinosus: 270 G bases, 36 runs, SRP367919 [34]) that separated RNA into three tissue sources (liver, colon, duodenum) using…”

Section: Candidates For Co-opted Filovirus-like Elementsmentioning

confidence: 99%

Genomic transfers help to decipher the ancient evolution of filoviruses and interactions with vertebrate hosts

Taylor,

Barnhart

2023

Preprint

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Although several filoviruses are dangerous human pathogens, there is conflicting evidence regarding their origins and interactions with animal hosts. Here we attempt to improve this understanding using the paleoviral record over a geological time scale, protein structure predictions, tests for evolutionary maintenance, and phylogenetic methods that alleviate sources of bias and error. We found evidence for long branch attraction bias in the L gene tree for filoviruses, and that using codon-specific models and protein structural comparisons of paleoviruses ameliorated conflict and bias. We found evidence for four ancient filoviral groups, each with extant viruses and paleoviruses with open reading frames. Furthermore, we found evidence of repeated transfers of filovirus-like elements to mouse-like rodents. A filovirus-like nucleoprotein ortholog with an open reading frame was detected in three subfamilies of spalacid rodents (present since the Miocene). These elements were unique among the detected filovirus-like paleoviruses in possessing open reading frames, expression products, and evidence for purifying selection. Our finding of structural conservation over geological time for paleoviruses informs virus and paleovirus discovery methods. Our results resolve a deep conflict in the evolutionary framework for filoviruses and reveal that genomic transfers to vertebrate hosts with potentially functional co-options have been more widespread than previously appreciated.Author SummaryFiloviruses are a family of RNA viruses discovered in 1967 and notorious for spillover of the dangerous pathogens, Ebola virus and Marburg virus. However, their origins, deeper relations, diversity, and interactions with animal hosts remain controversial. Part of the confusion may be that differing rates of evolution among divergent viral lineages can create a bias termed long branch attraction (LBA). We tested for this scenario in the L protein gene sequence of filoviruses and found evidence that LBA is occurring leading to a false pairing of filovirus lineages associated with a fish and a snake. We found that using nucleotides instead of amino acids when inferring trees, paleoviral sequences with open reading frames, additional conserved genes, and comparisons of predicted protein structures can resolve the LBA. We found four major groups of filoviruses, with the paleoviral record and trees being consistent with a fish origin for the family. Moreover, we found evidence of a filovirus-like element in spalacid rodents that has been evolutionarily maintained at the open-reading frame, amino acid sequence and structural level for over 20 million years. This element was also expressed in the liver, a target of filoviral infections. We conclude that genomic interactions of filoviruses with vertebrates, including the co-option of viral genes, are more important than previously appreciated.

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Adaptation of gut microbiome and host metabolic systems to lignocellulosic degradation in bamboo rats

Cited by 25 publications

References 90 publications

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons

Gut microbiome responds compositionally and functionally to the seasonal diet variations in wild gibbons

Metabolic Fate of Lignin in Birch Glucuronoxylan Extracts as Dietary Fiber Studied in a Rat Model

Genomic transfers help to decipher the ancient evolution of filoviruses and interactions with vertebrate hosts

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