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Diversity and novelty of the gut microbial community of an herbivorous rodent (Neotoma bryanti)
Abstract and Figures
Mammalian herbivores host diverse microbial communities to aid in fermentation and potentially detoxification of dietary compounds.
However, the microbial ecology of herbivorous rodents, especially within the largest superfamily of mammals (Muroidea) has
received little attention. We conducted a preliminary inventory of the intestinal microbial community of Bryant’s woodrat
(Neotoma bryanti), an herbivorous Muroidea rodent. We collected woodrat feces, generated 16S rDNA clone libraries, and obtained sequences
from 171 clones. Our results demonstrate that the woodrat gut hosts a large number of novel microorganisms, with 96% of the
total microbial sequences representing novel species. These include several microbial genera that have previously been implicated
in the metabolism of plant toxins. Interestingly, a comparison of the community structure of the woodrat gut with that of
other mammals revealed that woodrats have a microbial community more similar to foregut rather than hindgut fermenters. Moreover,
their microbial community was different to that of previously studied herbivorous rodents. Therefore, the woodrat gut may
represent a useful resource for the identification of novel microbial genes involved in cellulolytic or detoxification processes.
Keywords16S rDNA–Detoxification–Intestinal microbes–Mammalian herbivore–
Neotoma bryanti
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... It is obvious that it is impossible to decipher the adaptation of animals to changing environments using only morphoecological approaches. An understanding of the functional role of the intestinal microbiota in different aspects of the host's life has emerged only in the past two decades due to the use of microbiological, biochemical, and other research methods (Kohl et al., 2011;Kohl and Carey, 2016). ...
... This fact could be con-sidered as an important mechanism of adaptation to the food composition. The differences in the microbiota composition in phytophagous mammals of different taxa were also found using molecular genetic methods (Kohl et al., 2011). Microbial communities of the digestive tract are also known as a natural buffer for digestion under conditions of seasonal fluctuations in the quality of forage plants (Fon and Nsachlai, 2012). ...
We examine possible ways of functional adjustment of morphologically similar alimentary tracts in rodents with different dietary specializations. We study the structure of stomach and gut epithelial surface as well as the features of its colonization with microorganisms in five gerbil species: Psammomys obesus, Meriones crassus, Gerbillus henleyi, G. andersoni , and G. dasyurus . Data on the morphological diversity of mucosa-associated microbiota have been obtained and confirmed by the results of previous microbiology studies. Species differences in chymus acidity associated with dietary specialization have been determined. Variations in the activity of the endoglucanase microbial enzyme, which is crucial for rodents fed on cellulose-containing food, have also been detected. The importance of microbiota for functional adaptations to various food types in rodents with morphologically similar digestive tracts has been evaluated.
... Among those, the most abundant species can be attributed to Lactococcus lactis (21.2%), Serratia marcescens (10.6%), and Pseudomonas vranovensis (13.4%), which have been proved to effectively remove tannin [48,52,59,65,83]. As tannins are anti-nutrient to a wide range of insects and mammalian herbivores or even birds [46,63,76,82,113], bacterial genera with tannase activity found in the gut samples imply that C. arakawai larvae must have evolved adaptive mechanisms to detoxify or tolerate high-level tannins, as weevil larvae are prominent infested vectors in acorns of various oak species [90,99,109,111]. ...
... It has been well accepted that the gut microbiota of mammals performs an immense range of functions that benefit the host's development, nutrition, physiology, and pathogen resistance [51,52,64,77]. Our results showed that ingestion of unsterilized C. arakawai larvae significantly altered the gut microbial community membership and structure of T. sibiricus (see also Figs. ...
Gut microbiota can be transmitted either environmentally or socially and vertically at intraspecific level; however, whether gut microbiota interact along trophic levels has been largely overlooked. Here, we characterized the gut bacterial communities of weevil larvae of Curculio arakawai that infest acorns of Mongolian oak (Quercus mongolica) as well as acorn-eating mammals, Siberian chipmunk (Tamias sibiricus), to test whether consumption of seed-borne larvae remodels the gut bacterial communities of T. sibiricus. Ingestion of weevil larvae of C. arakawai significantly altered the gut bacterial communities of T. sibiricus. Consequently, T. sibiricus fed larvae of C. arakawai showed higher capability to counter the negative effects of tannins, in terms of body weight maintenance, acorn consumption, N content in feces, urine pH, and blood ALT activity. Our results may first show that seed-borne insects as hidden players have a potential to alter the gut microbiota of seed predators in the tripartite system.
... The previous report showed that intestinal microbiome plays an important role in digestion and absorption of the food, and maintaining animals' health 21,22 . Intestinal tracts of the ruminants are rich in symbiotic bacteria that helps the body digest plant fibers 23,24 . Glycans are processed by the distal gut microbiota, generating biologically significant short-chain fatty acids (SCFAs, predominantly acetate, butyrate, and propionate), which serve as the principal energy source for colonocytes 25 . ...
Yaks and Tibetan sheep are important and renowned livestock of the Qinghai-Tibetan Plateau (QTP). Both host genetics and environmental factors can shape the composition of gut microbiota, however, there is still no consensus on which is the more dominant factor. To investigate the influence of hosts and seasons on the gut microbiome diversity component, we collected fecal samples from yaks and Tibetan sheep across different seasons (summer and winter), during which they consumed different diets. Using 16S rRNA sequencing, principal component analysis (PCoA) data showed that PCo1 explained 57.4% of the observed variance (P = 0.001) and clearly divided winter samples from summer ones, while PCo2 explained 7.1% of observed variance (P = 0.001) and mainly highlighted differences in host species. Cluster analysis data revealed that the gut microbiota composition displayed a convergence caused by season and not by genetics. Further, we profiled the gut microbial community and found that the more dominant genera in yak and Tibetan sheep microbiota were influenced by seasonal diets factors rather than genetics. This study therefore indicated that seasonal diet can trump host genetics even at higher taxonomic levels, thus providing a cautionary note for the breeding and management of these two species.
... Once the growth is excessive, they become pathogenic and injure the body. Several researchers have found that the structure and diversity of the intestinal microbial community are closely related to species [8] animal age [9] and growth environment [10]. Meng found that weaning transition can change the proportion and structure of microbiota [11]. ...
Background
In order to study the influence of long-term growth process and evolution environment on intestinal bacteria of different breeds, the intestinal bacteria and volatile fatty acids among the faeces of Min, Landrace and Yorkshire pigs were analysed by Illumina high-throughput sequencing of the 16S-rDNA and gas chromatography.
Results
The shared core microbiota of Landrace, Yorkshire and Min pig were 1273, accounting for 69.56% of total abundance of organisms. The proportion of Firmicutes in Min pig faeces (57.89%) was significantly higher than that in Landrace and Yorkshire pig faeces (47.01% and 46.40%, respectively) (P < 0.05), but that of Bacteroidetes was exactly opposite. Moreover, Min pig presented more highly efficient membrane transport, environmental adaptation, carbohydrate transport, and metabolism than Yorkshire pig (P < 0.05). The acetic acid/total volatile fatty acid ratio in Min pig was significantly higher than that in Landrace pig (P < 0.05), and the isobutyric acid/ total volatile fatty acid ratio in Min pig was significantly larger than that in Yorkshire pig (P < 0.05). Furthermore, the content of branched chain volatile fatty acids in Min pig was significantly higher than that in Yorkshire pig (P < 0.05).
Conclusions
This study demonstrated that Min pig, as an excellent breed in the cold area of China, possessed special intestinal floral structure compared to the imported pigs in order to satisfy their physiological and metabolic demands, which may influence their characteristics such as resistance to cold, diseases, and crude feeding, and the ability to deposit intramuscular fat.
How to cite: Yang Y, Sun C, Li F, et al. Characteristics of faecal bacterial flora and volatile fatty acids in Min pig, Landrace pig, and Yorkshire pig. Electron J Biotechnol 2021;52. https://doi.org/10.1016/j.ejbt.2021.05.002
... A close relationship exists between the host and the flora in the intestine. Breeds (Kohl et al., 2011), Food (Chen et al., 2011) and living environment (Wu et al., 2012) can affect the composition and function of intestinal flora. Moreover, intestinal flora changes can affect the nutrition of the organism (Turnbaugh et al., 2006), organ function (Benson et al., 2010) and immune status (Danielsen et al., 2007). ...
... There is an expanding literature addressing the roles of the microbiota in terrestrial vertebrates (e.g., Dierenfeld et al.1982;Ley et al. 2008;Russell et al. 2009;Kohl et al. 2011;Zhao et al. 2013;Kohl and Dearing 2014); however, there are fewer studies investigating this topic in fishes (e.g., Rimmer and Wiebe 1987;Mountfort et al. 2002;Moran et al. 2005;Nayak 2010;Givens et al. 2015;Liu et al. 2016;Egerton et al. 2018;Earley et al. 2018;Escalas et al. 2021). Fishes represent the largest taxonomic group of vertebrates on the planet and thus, their impact on ecosystem functions around the globe are vast (e.g., Choat and Clements 1998;Karasov and Martinez del Rio 2007;Cortés et al. 2008;Bucking 2016;Leigh et al. 2017). ...
The intestinal microbiome of vertebrates has been shown to play a crucial role in their digestive capabilities. This is particularly true for omnivores and herbivores that rely on enteric microbes to digest components of plant material that are indigestible by host-derived enzymes. While studies of microbe-host interactions are becoming more frequent in terrestrial systems, studies of this type are still limited in marine systems, particularly for higher trophic level organisms. Although sharks are largely carnivorous, the bonnethead shark (Sphyrna tiburo) has been identified as an omnivore, given that it assimilates seagrass material in addition to proteinaceous prey items such as crustaceans. The mechanisms by which bonnetheads digest seagrass, including microbial digestion, are still unknown. We use digestive enzyme assays, histological imaging, measurements of microbial fermentation, and 16S rDNA sequencing to explore potential processes by which the bonnethead shark may digest and assimilate plant material. We found evidence of microbial fermentation (as evident by moderate short-chain-fatty-acid concentrations) as well as evidence of greater epithelial surface area in their spiral intestine compared to other gut regions. We identified specific orders of microbes that make up the majority of the bonnethead shark gut microbiome (Vibrionales, Clostridiales, Pseudomonadales, Mycoplasmatales, Rhizobiales, and others), some of which are known, in other organisms, to be involved in the production of enzymes responsible for the breakdown of chitin (found in crustacean shells) and components of cellulose (found in seagrass). Our results highlight that an organism from a stereotypical “carnivorous” group is capable of breaking down seagrass, including potential for some fiber degradation, as well as advances our knowledge of gut microbe community structure in sharks.
... In addition, almost nothing is known about microbial diversity in the digestive system of these cricetids. In two neotomines with bilocular stomachs (Neotoma bryanti and Neotoma albigula- Kohl et al. 2011Kohl et al. , 2014, bacterial richness estimated for the stomach was similar to that detected in the caecum and large intestine, highlighting the importance of the bacterial community for the initial digestion of fiber, recycling of endogenous nitrogen, and detoxification of dietary toxins. This is a subject that requires attention to illuminate the physiological evolution of digestion in sigmodontines (Domínguez-Bello and Robinson 1991). ...
Akodontini, the second largest tribe within sigmodontine rodents, encompasses several stomach morphologies. This is striking because most sigmodontine groups of comparable taxonomic rank are very conservative in this respect. Based on extensive sampling of newly dissected specimens (213 stomachs representing 36 species), as well as published examples, covering almost all akodontine living genera (15 of 16), we undertook a reappraisal of the gross morphology of this organ. We then mapped this information, together with gallbladder occurrence, in a refined multilocus molecular phylogeny of the tribe. We surveyed three different configurations of stomachs in akodontines, according to the degree of development and location of the glandular epithelium; in addition, two minor variations of one of these types were described. Of the five major clades that integrate Akodontini, four are characterized by a single stomach morphology, while one clade exhibits two morphologies. Mapping stomach type on the phylogeny recovered two configurations for the most recent ancestor of Akodontini. A revised survey of gallbladder evidence also revealed overlooked congruencies. The observed stomach diversity and its arrangement in the phylogeny, along with additional morphological characters and the genetic diversity among the main clades, supports the necessity of changes in the current classification of the tribe. Recognition of subtribes or partitioning of Akodontini into several additional tribes of equal rank could be suitable options.
... The adaptive modulation hypothesis [17] suggests a positive correlation between digestive enzyme activities and ingested quantity of the substrate for those enzymes. Based on economic principles, this hypothesis is well supported in the literature for carbohydrases, as herbivorous and omnivorous animals tend to have elevated amylase activities in their guts [11,[18][19][20][21][22][23], and achieve these activities largely via gene duplications [22]. The nutrient balancing hypothesis [24] suggests that there can be elevated expression of enzymes towards limiting dietary resources to ensure acquisition of essential nutrients, like essential fatty acids. ...
Adopting a new diet is a significant evolutionary change, and can profoundly affect an animal's physiology, biochemistry, ecology and genome. To study this evolutionary transition, we investigated the physiology and genomics of digestion of a derived herbivorous fish, Cebidichthys violaceus. We sequenced and assembled its genome (N50 = 6.7 Mb) and digestive transcriptome, and revealed the molecular changes related to digestive enzymes (carbohydrases, proteases and lipases), finding abundant evidence of molecular adaptation. Specifically, two gene families experienced expansion in copy number and adaptive amino acid substitutions: amylase and carboxyl ester lipase (cel), which are involved in the digestion of carbohydrates and lipids, respectively. Both show elevated levels of gene expression and increased enzyme activity. Because carbohydrates are abundant in the prickleback's diet and lipids are rare, these findings suggest that such dietary specialization involves both exploiting abundant resources and scavenging rare ones, especially essential nutrients, like essential fatty acids.
... TM7 bacteria are found in diverse habitats like soil, freshwater, human oral cavity, gut of several animals, etc. (Marcy et al., 2007;Kuehbacher et al., 2008;Ferrari et al., 2014); however, the functional attributes of TM7 phylum remain largely unknown. Some members of TM7 have been suggested to presumably play a role in the degradation of polyphenols in the gut of woodrat (Kohl et al., 2011). Therefore, the reduction of TM7 may affect the digestion efficiency of captive and domestic populations as polyphenols; in particular, tannins at higher concentrations are reported to reduce the nutrient absorption in ruminants (Frutos et al., 2004). ...
Although gut microbiome benefits the host in several ways, how anthropogenic forces impact the gut microbiome of mammals is not yet completely known. Recent studies have noted reduced gut microbiome diversity in captive mammals due to changes in diet and living environment. But, no studies have been carried out to understand how gut microbiome of wild mammals responds to domestication. We analysed the gut microbiome of wild and captive gaur and domestic mithun (domestic form of gaur) to understand whether the gut microbiome exhibits sequential changes from wild to captivity and after domestication. Both captive and domestic populations were characterized by reduced microbial diversity and abundance as compared to their wild counterparts. Notably, two beneficial bacterial families Ruminococcaceae and Lachnospiraceae, which are known to play vital roles in herbivores’ digestion, exhibited lower abundance in captive and domestic populations. Consequently, the predicted bacterial functional pathways especially related to metabolism and immune system showed lower abundance in captive and domestic populations compared to wild population. Therefore, we suggest that domestication can impact the gut microbiome more severely than captivity which might lead to adverse effects on host health and fitness. However further investigations are required across a wide range of domesticates in order to understand the general trend of microbiome shifts in domestic animal.
... Compared with the carnivores, gastric and intestinal tracts of the ruminants are rich in symbiotic bacteria that helps the body digest plant fibers (Kohl et al., 2011;Muegge et al., 2011;Saro et al., 2012;Kim et al., 2013). The development of a rumen is driven by close interactions among the rumens, metabolic products of microorganisms, diet and the host . ...
As for the wild animals, their diet components are always changed, so that we have to monitor such changes by analyzing the modification of intestinal microbial community. Such effort allows us to amend their conservation strategies and tactics accordingly so that they are able to appropriately adapt to the new environment and dietary selection. In this study we focus on the gut flora of two groups of an endangered species, Alpine musk deer (Moschus chrysogaster), wild group (WG) which is compared with that of the individuals of the same species but kept in the captivities (CG), a control group. Such a project is aimed to work out whether the composition of the gut microbes has significantly been changed due to captive feedings. To do so, we used 16S rRNA amplicon sequencing to characterize gut bacteria of the musk deer from the two groups. The results show that there is a significant difference in community structure of the bacteria: WG shows significant enrichment of Firmicutes and depletion of Bacteroidetes, while CG has a significant abundance of Proteobacteria and Euryarchaeota. Metagenomics was used to analyze the differences in functional enzymes between the two groups. The related results indicate that genes in WG are mostly related to the enzymes digesting cellulose and generating short-chain fatty acids (SCFAs) for signaling pathways, but CG shows enrichment in methanogenesis, including the CO2/H2 pathway and the methylotrophic pathway. Thus, this study indicates that the Firmicutes-rich gut microbiota in the WG enables individuals to maximize their energy intake from the cellulose, and has significant abundance of Euryarchaeota and methanogenesis pathways that allow them to reduce redundant energy consumption in methane metabolism, ensuring them to adapt to the wild environments.
Nutrition and toxicology are closely intertwined. Toxic substances can interfere with vital functions of the gastrointestinal tract such as digestion, absorption, excretion, and their regulatory control. From a toxicology viewpoint animals are continually challenged by compounds that are without nutritive value — material that they nevertheless ingest, inhale, or absorb. Such exposure to toxic compounds has been going on as long as life has and is not merely a consequence of the modern era of industrialization. In fact, toxin production may be considered a successful evolutionary strategy or adaptation to predators or a form of chemical warfare practiced by species as varied as insects, frogs, and plants (Rosenthal and Janzen 1979).
The nutritional ecology of desert wood rats was studied at a site in the Mojave Desert that lacked succulents. During the late fall and early winter, before winter rains, wood rats ate primarily mature leaves and stems of creosote bush Larrea tridentata, whereas after winter rains they ate newly germinating annuals. Wood rats were apparently deterred from eating enough Larrea to satisfy energy requirements by Larrea's high resin content, but their need to maintain water balance probably precluded them from relying heavily on other plant species, all of which contain less water. Thus, until the winter rains and the germination of annuals, wood rats suffered mass decreases and some probably died. -from Author
A rumen isolate, Coprococcus, sp. Pe(1)5, was found to carry phloroglucinol reductase, which catalyzed the initial step in the breakdown of phloroglucinol. The organism uses phloroglucinol as the sole source of carbon and energy when grown in the absence of oxygen. Induced levels of enzyme were detected in cells grown either on phloroglucinol or on other carbon sources in the presence of limiting quantities of phloroglucinol. Although the organism is a strict anaerobe, the enzyme from anaerobically grown cells was insensitive to air. The partially purified enzyme required reduced nicotinamide adenine dinucleotide phosphate as an electron donor and was specific for phloroglucinol. However, partial enzyme activity (14 to 17%) was also detected in the presence of 2-methyl-1,4-naphthoquinone but not in the presence of several other phenolic compounds. The enzyme exhibited a higher affinity for phloroglucinol than for reduced nicotinamide adenine dinucleotide phosphate, with K(m) values of 3.0 x 10 M and 29.0 x 10 M, respectively. The optimum pH for maximal enzyme activity was 7.4, and the molecular weight of the native protein was about 130,000, as determined by the Sephadex gel filtration technique.
The rate and extent of degradation of plant structural tissues during digestion depends on a combination of animal, plant, and microbial factors. The major animal effect is the nature of the digestive tract itself. Ruminants with pregastric ruminai fermentation generally have a lower rate of passage than is seen in monogastric animals, and rumination (regurgitation and remastication) of large particles permits them to macerate fibrous materials more completely than do monogastric animals. Ruminants are thus more efficient at digesting fibrous plant material than are monogastric animals, in which fermentation occurs only in the large intestine. In contrast to ruminants, monogastric animals often tend to consume more readily digestible feeds. For example, cereals are a major component of the diets commonly fed to domestic animals. Thus, there is often a quantitative compositional difference in the substrates available to the digestive microbiota present in ruminants and monogastric animals. Cellulolytic organisms which are of pivotal importance in the rumen are generally viewed to have a lesser role than other fermentative organisms in the postgastric intestinal fermentation of domestic animals; however, there are exceptions — for example, the horse. Undoubtedly the presence or absence of particular gut species is directly related to the diet consumed and the retention time of the system.
During winter, creosote bush dominates the diet of desert woodrats in the California Mojave Desert. Stems and leaves of creosote foliage are coated with large quantites of phenolic resins (10-25% of dry mass). Woodrats consistently selected creosote plant parts of low resin content. The antiherbivore mechanism of creosote resin to desert woodrats is likely one of toxicity and not digestibility reduction. This toxicity may limit the amount of creosote foliage woodrats can consume, which would explain the winter body mass decline and mortality observed on the study site. -from Authors