Gut microbes of mammalian herbivores facilitate intake of plant toxins

Kohl, Kevin D.; Weiss, Robert B.; Cox, James E.; Dale, Colin; Dearing, M. Denise

doi:10.1111/ele.12329

Cited by 252 publications

(274 citation statements)

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“…In addition to having a role in fermentation, microbes play an important role in the biotransformation of dietary toxins in mammalian herbivores (4,(7)(8)(9)(10). For some toxins, such as oxalate or 3,4-dihydroxypyridine (DHP), a single species of bacteria is capable of biotransforming the toxin, and this function can be transferred to other mammals through microbial transplants (7,8,11,12).…”

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confidence: 99%

“…For some toxins, such as oxalate or 3,4-dihydroxypyridine (DHP), a single species of bacteria is capable of biotransforming the toxin, and this function can be transferred to other mammals through microbial transplants (7,8,11,12). For other toxins, such as creosote resin, whole microbial community transplantation into other mammals can increase tolerance (10).…”

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confidence: 99%

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Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula

Miller

Oakeson

Dale

et al. 2016

Appl Environ Microbiol

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Diet is one of the primary drivers that sculpts the form and function of the mammalian gut microbiota. However, the enormous taxonomic and metabolic diversity held within the gut microbiota makes it difficult to isolate specific diet-microbe interactions. The objective of the current study was to elucidate interactions between the gut microbiota of the mammalian herbivore Neotoma albigula and dietary oxalate, a plant secondary compound (PSC) degraded exclusively by the gut microbiota. We quantified oxalate degradation in N. albigula fed increasing amounts of oxalate over time and tracked the response of the fecal microbiota using high-throughput sequencing. The amount of oxalate degraded in vivo was linearly correlated with the amount of oxalate consumed. The addition of dietary oxalate was found to impact microbial species diversity by increasing the representation of certain taxa, some of which are known to be capable of degrading oxalate (e.g., Oxalobacter spp.). Furthermore, the relative abundances of 117 operational taxonomic units (OTU) exhibited a significant correlation with oxalate consumption. The results of this study indicate that dietary oxalate induces complex interactions within the gut microbiota that include an increase in the relative abundance of a community of bacteria that may contribute either directly or indirectly to oxalate degradation in mammalian herbivores. Mammals live in a complex and largely symbiotic relationship with their gut microbiota. This microbiota harbors 150 times more genes than the host and exhibits complex interactions with the host's diet (1-3). In mammalian herbivores, diverse intestinal bacteria ferment a diet high in recalcitrant cellulose and in turn synthesize nutrients from the diet in a form more amenable to absorption by the host (4). Furthermore, mammalian herbivores harbor greater microbial diversity in their gut than either omnivores or carnivores (1). Despite the progress of research into the interactions between the mammalian gut microbiota and diet, the isolation of specific diet-microbe interactions in such a complex system has proven to be difficult (5, 6).In addition to having a role in fermentation, microbes play an important role in the biotransformation of dietary toxins in mammalian herbivores (4, 7-10). For some toxins, such as oxalate or 3,4-dihydroxypyridine (DHP), a single species of bacteria is capable of biotransforming the toxin, and this function can be transferred to other mammals through microbial transplants (7,8,11,12). For other toxins, such as creosote resin, whole microbial community transplantation into other mammals can increase tolerance (10).Oxalate, a widely produced and ingested plant secondary compound (PSC), serves as an excellent model to study diet-microbe interactions (13). It is the simplest organic acid and is toxic to mammals (14-16). Oxalate can bind to free calcium ions in the blood and aggregate in the kidneys to form kidney stones (17). In fact, oxalate is a constituent in 80% of kidney stones in humans (17). Oxala...

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confidence: 99%

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confidence: 99%

Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula

Miller

Oakeson

Dale

et al. 2016

Appl Environ Microbiol

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“…Recent work in herbivorous rodents (woodrats) has demonstrated that the gut microbiota is instrumental in allowing the animals to safely ingest toxin-rich plants (Kohl and Dearing, 2016). For example, reduction of the gut microbiota with antibiotics significantly impairs woodrats' abilities to consume PSCs (Kohl et al, 2014c). Remarkably, the toxin-degrading functions bestowed upon hosts by the gut microbiota can be readily transferred across populations and host species through microbial transplants (Kohl et al, 2016b,c;Miller et al, 2016a).…”

Section: Animal-microbe Symbioses Contribute To Host Ecology and Evolmentioning

confidence: 99%

“…Unfortunately, generating germ-free animals can be highly challenging for studies with non-laboratory terrestrial vertebrates, especially if they are difficult to maintain or manipulate in captivity, or the question of interest must be asked and studied in the field. That said, microbial transplants have been performed between wild-caught rodents (Kohl et al, 2014c) and antibiotic treatments have been administered to penguins in the field (Potti et al, 2002). Creative solutions tailored to specific study systems will be required to advance our knowledge of how hostmicrobiome symbioses affect the physiology, ecology and evolution of individual animals and their populations.…”

Section: Animal-microbe Symbioses Contribute To Host Ecology and Evolmentioning

confidence: 99%

A place for host–microbe symbiosis in the comparative physiologist's toolbox

Kohl

Carey

2016

Journal of Experimental Biology

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Although scientists have long appreciated that metazoans evolved in a microbial world, we are just beginning to appreciate the profound impact that host-associated microbes have on diverse aspects of animal biology. The enormous growth in our understanding of hostmicrobe symbioses is rapidly expanding the study of animal physiology, both technically and conceptually. Microbes associate functionally with various body surfaces of their hosts, although most reside in the gastrointestinal tract. Gut microbes convert dietary and host-derived substrates to metabolites such as short-chain fatty acids, thereby providing energy and nutrients to the host. Bacterial metabolites incorporated into the host metabolome can activate receptors on a variety of cell types and, in doing so, alter host physiology (including metabolism, organ function, biological rhythms, neural activity and behavior). Given that host-microbe interactions affect diverse aspects of host physiology, it is likely that they influence animal ecology and, if they confer fitness benefits, the evolutionary trajectory of a species. Multiple variables -including sampling regime, environmental parameters, host metadata and analytical methods -can influence experimental outcomes in host-microbiome studies, making careful experimental design and execution crucial to ensure reproducible and informative studies in the laboratory and field. Integration of microbiomes into comparative physiology and ecophysiological investigations can reveal the potential impacts of the microbiota on physiological responses to changing environments, and is likely to bring valuable insights to the study of host-microbiome interactions among a broad range of metazoans, including humans.

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“…Accordingly, animal evolution has widely featured adaptations to ecosystems shaped by bacteria (McFall-Ngai et al, 2013), as well as interactions with bacteria that affect animals' responses to other environmental factors. Bacteria can protect animals and their embryonic stages from pathogens (Gil-Turnes et al, 1989), heavy metal pollution (Senderovich and Halpern, 2013;Breton et al, 2013), or toxic secondary compounds in plant diets (Kohl et al, 2014); conversely, they can convert xenobiotics into more harmful forms (Freeland and Janzen, 1974;Zheng et al, 2013). Bacteria can provide crucial signals about the environment, as in the case of marine tubeworm larvae that use molecules from surface-associated bacteria as cues to settle and metamorphose (Shikuma et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

Mushegian

Burcklen

Schär

et al. 2016

Journal of Experimental Biology

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The environments in which animals develop and evolve are profoundly shaped by bacteria, which affect animals both indirectly through their role in biogeochemical processes and directly through antagonistic or beneficial interactions. The outcomes of these activities can differ according to environmental context. In a series of laboratory experiments with diapausing eggs of the water flea Daphnia magna, we manipulated two environmental parameters, temperature and presence of bacteria, and examined their effect on development. At elevated temperatures (≥26°C), resting eggs developing without live bacteria had reduced hatching success and correspondingly higher rates of severe morphological abnormalities compared with eggs with bacteria in their environment. The beneficial effect of bacteria was strongly reduced at 20°C. Neither temperature nor the presence of bacteria affected directly developing parthenogenetic eggs. The mechanistic basis of this effect of bacteria on development is unclear, but these results highlight the complex interplay of biotic and abiotic factors influencing animal development after diapause.

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Gut microbes of mammalian herbivores facilitate intake of plant toxins

Cited by 252 publications

References 40 publications

Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula

Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula

A place for host–microbe symbiosis in the comparative physiologist's toolbox

Temperature-dependent benefits of bacterial exposure in embryonic development of Daphnia magna resting eggs

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