Metatranscriptomic Analyses Reveal Important Roles of the Gut Microbiome in Primate Dietary Adaptation

The gut microbiome plays a vital role in host ecological adaptation, especially dietary adaptations. Primates have evolved a variety of dietary and gut physiological structures that are useful to explore the role of the gut microbiome in host dietary adaptations. Here, we characterize gut microbiome transcriptional activity in ten fecal samples from primates with three different diets and compare the results to their previously reported metagenomic profile. Bacteria related to cellulose degradation, like Bacteroidaceae and Alcaligenaceae, were enriched and actively expressed in the gut microbiome of folivorous primates, and functional analysis revealed that the glycan biosynthesis and metabolic pathways were significantly active. In omnivorous primates, Helicobacteraceae, which promote lipid metabolism, were significantly enriched in expression, and activity and xenobiotic biodegradation and metabolism as well as lipid metabolism pathways were significantly active. In frugivorous primates, the abundance and activity of Elusimicrobiaceae, Neisseriaceae, and Succinivibrionaceae, which are associated with digestion of pectin and fructose, were significantly elevated, and the functional pathways involved in the endocrine system were significantly enriched. In conclusion, the gut microbiome contributes to host dietary adaptation by helping hosts digest the inaccessible nutrients in their specific diets.

[1]  Zuofu Xiang,et al.  The Relationship Between Gut Microbiome and Bile Acids in Primates With Diverse Diets , 2022, Frontiers in Microbiology.

[2]  B. Camacho-Zamora,et al.  Maternal Sweeteners Intake Modulates Gut Microbiota and Exacerbates Learning and Memory Processes in Adult Male Offspring , 2022, Frontiers in Pediatrics.

[3]  P. Gajer,et al.  Insight into the ecology of vaginal bacteria through integrative analyses of metagenomic and metatranscriptomic data , 2021, bioRxiv.

[4]  S. Lee,et al.  High-fiber diets attenuate emphysema development via modulation of gut microbiota and metabolism , 2021, Scientific Reports.

[5]  S. Nie,et al.  Deciphering diet-gut microbiota-host interplay: Investigations of pectin , 2020 .

[6]  M. Goran,et al.  Lactose-reduced infant formula with added corn syrup solids is associated with a distinct gut microbiota in Hispanic infants , 2020, Gut microbes.

[7]  R. Junge,et al.  A role for gut microbiota in host niche differentiation , 2020, The ISME Journal.

[8]  T. Spector,et al.  Effect of Diet on the Gut Microbiota: Rethinking Intervention Duration , 2019, Nutrients.

[9]  Bruce D. Patterson,et al.  Ecology and Host Identity Outweigh Evolutionary History in Shaping the Bat Microbiome , 2019, mSystems.

[10]  R. Pringle,et al.  Covariation of diet and gut microbiome in African megafauna , 2019, Proceedings of the National Academy of Sciences.

[11]  C. Knauf,et al.  The gut microbiome influences host endocrine functions. , 2019, Endocrine reviews.

[12]  G. Siuzdak,et al.  A fiber-deprived diet disturbs the fine-scale spatial architecture of the murine colon microbiome , 2019, Nature Communications.

[13]  Patrick S. G. Chain,et al.  Advances and Challenges in Metatranscriptomic Analysis , 2019, Front. Genet..

[14]  Baohua Xu,et al.  The different dietary sugars modulate the composition of the gut microbiota in honeybee during overwintering , 2019, BMC Microbiology.

[15]  K. Kohl,et al.  Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices , 2019, Proceedings of the Royal Society B.

[16]  Aaron W. Miller,et al.  Metagenomic sequencing provides insights into microbial detoxification in the guts of small mammalian herbivores (Neotoma spp.) , 2018, FEMS microbiology ecology.

[17]  L. Jespersen,et al.  Modulation of gut microbiota from obese individuals by in vitro fermentation of citrus pectin in combination with Bifidobacterium longum BB-46 , 2018, Applied Microbiology and Biotechnology.

[18]  Huajun Zhang,et al.  Microbial Community Dynamics and Assembly Follow Trajectories of an Early-Spring Diatom Bloom in a Semienclosed Bay , 2018, Applied and Environmental Microbiology.

[19]  D. Raubenheimer,et al.  Macronutrient signature of dietary generalism in an ecologically diverse primate in the wild , 2018 .

[20]  J. Rothman,et al.  Nutritional composition of the diet of the northern yellow-cheeked crested gibbon (Nomascus annamensis) in northeastern Cambodia , 2018, Primates.

[21]  Yong-guan Zhu,et al.  Linking Genes to Microbial Biogeochemical Cycling: Lessons from Arsenic. , 2017, Environmental science & technology.

[22]  E. Balskus,et al.  Chemical transformation of xenobiotics by the human gut microbiota , 2017, Science.

[23]  T. Sharpton,et al.  Increasing dietary nitrate has no effect on cancellous bone loss or fecal microbiome in ovariectomized rats , 2017, Molecular nutrition & food research.

[24]  E. Alm,et al.  Unraveling the processes shaping mammalian gut microbiomes over evolutionary time , 2017, Nature Communications.

[25]  M. Shapira Gut Microbiotas and Host Evolution: Scaling Up Symbiosis. , 2016, Trends in ecology & evolution.

[26]  M. Huffman,et al.  Marked variation between winter and spring gut microbiota in free-ranging Tibetan Macaques (Macaca thibetana) , 2016, Scientific Reports.

[27]  G. Dehnhardt,et al.  Comparative analysis of the fecal bacterial community of five harbor seals (Phoca vitulina) , 2016, MicrobiologyOpen.

[28]  Eran Elinav,et al.  Use of Metatranscriptomics in Microbiome Research , 2016, Bioinformatics and biology insights.

[29]  Y. Koh,et al.  High-fat-diet-modulated Gut Microbiota Promotes Intestinal Carcinogenesis , 2015 .

[30]  J. Jansson,et al.  Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies , 2015, Front. Microbiol..

[31]  A. Rodrigo,et al.  Patterns of Gut Bacterial Colonization in Three Primate Species , 2015, PloS one.

[32]  N. Blom,et al.  The microbiome of New World vultures , 2014, Nature Communications.

[33]  Ming Li,et al.  Whole-genome sequencing of the snub-nosed monkey provides insights into folivory and evolutionary history , 2014, Nature Genetics.

[34]  William D Hopkins,et al.  Why primate models matter , 2014, American journal of primatology.

[35]  Haixu Tang,et al.  Gene finding in metatranscriptomic sequences , 2014, BMC Bioinformatics.

[36]  P. West,et al.  Deciphering microbial landscapes of fish eggs to mitigate emerging diseases , 2014, The ISME Journal.

[37]  T. Junt,et al.  Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis , 2014, Nature Medicine.

[38]  J. A. Encarnação,et al.  Insectivorous Bats Digest Chitin in the Stomach Using Acidic Mammalian Chitinase , 2013, PloS one.

[39]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[40]  Rafael Bargiela,et al.  Gut microbiota disturbance during antibiotic therapy: a multi-omic approach , 2012, Gut.

[41]  Hélène Touzet,et al.  SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data , 2012, Bioinform..

[42]  Zhengwei Zhu,et al.  CD-HIT: accelerated for clustering the next-generation sequencing data , 2012, Bioinform..

[43]  E. Martens,et al.  How glycan metabolism shapes the human gut microbiota , 2012, Nature Reviews Microbiology.

[44]  Qi Wu,et al.  Evidence of cellulose metabolism by the giant panda gut microbiome , 2011, Proceedings of the National Academy of Sciences.

[45]  Eoin L. Brodie,et al.  Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows , 2011, The ISME Journal.

[46]  Colin N. Dewey,et al.  RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome , 2011, BMC Bioinformatics.

[47]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[48]  N. Friedman,et al.  Trinity : reconstructing a full-length transcriptome without a genome from RNA-Seq data , 2016 .

[49]  Miguel Pignatelli,et al.  Metatranscriptomic Approach to Analyze the Functional Human Gut Microbiota , 2011, PloS one.

[50]  G. Hanya,et al.  Dietary adaptations of temperate primates: comparisons of Japanese and Barbary macaques , 2011, Primates.

[51]  Amy Lu,et al.  Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. , 2011, American journal of physical anthropology.

[52]  G. Perry,et al.  Evolutionary adaptations to dietary changes. , 2010, Annual review of nutrition.

[53]  S. Denman,et al.  Plant biomass degradation by gut microbiomes: more of the same or something new? , 2009, Current opinion in biotechnology.

[54]  Mark Johnson,et al.  NCBI BLAST: a better web interface , 2008, Nucleic Acids Res..

[55]  C. Peres Primate Conservation Biology Cometh of Age , 2001 .

[56]  T. Struhsaker Colobine monkeys. Their ecology, behaviour and evolution , 1995, International Journal of Primatology.

[57]  C. Janson,et al.  Morphological and behavioral adaptations for foraging in generalist primates: the case of the cebines. , 1992, American journal of physical anthropology.

[58]  W. Loesche,et al.  Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis , 1982, Infection and immunity.

[59]  S. E. West,et al.  Fermentation of mucin and plant polysaccharides by strains of Bacteroides from the human colon , 1977, Applied and environmental microbiology.

[60]  K. Amato Incorporating the gut microbiota into models of human and non-human primate ecology and evolution. , 2016, American journal of physical anthropology.

[61]  D. Mansuy [Metabolism of xenobiotics: beneficial and adverse effects]. , 2013, Biologie aujourd'hui.

[62]  Ya-ping Zhang,et al.  Adaptive evolution of digestive RNASE1 genes in leaf-eating monkeys revisited: new insights from ten additional colobines. , 2010, Molecular biology and evolution.

[63]  J. Fooden Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780) / Jack Fooden. , 2000 .

[64]  J. Lambert Primate digestion: Interactions among anatomy, physiology, and feeding ecology , 1998 .

[65]  D. Hill,et al.  Seasonal variation in the feeding behavior and diet of Japanese macaques (Macaca fuscata yakui) in lowland forest of Yakushima , 1997, American journal of primatology.