Signatures of landscape and captivity in the gut microbiota of Southern Hairy-nosed Wombats (Lasiorhinus latifrons)

Eisenhofer, Raphael; Helgen, Kristofer M.; Taggart, David A.

doi:10.1186/s42523-020-00068-y

Cited by 13 publications

(23 citation statements)

References 61 publications

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“…Many studies that measured microbial diversity report decreased gut richness or diversity in individuals in captivity compared to others in the wild [e.g. 22 , 35 , 36 ]. However, some studies have reported no difference in microbial diversity between the two environments [e.g.…”

Section: Review Of Current Literature On the Captive Microbiomementioning

confidence: 99%

“…There are alternative interpretations of microbial differences between wild and captive animals that do not presume the captive microbiome is less favorable [e.g. 35 , 86 – 88 ] or potentially detrimental [ 1 ]; these are important to consider in the absence of species-specific experimental evidence. First, microbiomes may have changed to match the new captive environment in a beneficial manner [ 89 ].…”

Section: Review Of Current Literature On the Captive Microbiomementioning

confidence: 99%

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Possibilities and limits for using the gut microbiome to improve captive animal health

Díaz

Reese

2021

anim microbiome

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Because of its potential to modulate host health, the gut microbiome of captive animals has become an increasingly important area of research. In this paper, we review the current literature comparing the gut microbiomes of wild and captive animals, as well as experiments tracking the microbiome when animals are moved between wild and captive environments. As a whole, these studies report highly idiosyncratic results with significant differences in the effect of captivity on the gut microbiome between host species. While a few studies have analyzed the functional capacity of captive microbiomes, there has been little research directly addressing the health consequences of captive microbiomes. Therefore, the current body of literature cannot broadly answer what costs, if any, arise from having a captive microbiome in captivity. Addressing this outstanding question will be critical to determining whether it is worth pursuing microbial manipulations as a conservation tool. To stimulate the next wave of research which can tie the captive microbiome to functional and health impacts, we outline a wide range of tools that can be used to manipulate the microbiome in captivity and suggest a variety of methods for measuring the impact of such manipulation preceding therapeutic use. Altogether, we caution researchers against generalizing results between host species given the variability in gut community responses to captivity and highlight the need to understand what role the gut microbiome plays in captive animal health before putting microbiome manipulations broadly into practice.

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Section: Review Of Current Literature On the Captive Microbiomementioning

confidence: 99%

Section: Review Of Current Literature On the Captive Microbiomementioning

confidence: 99%

Possibilities and limits for using the gut microbiome to improve captive animal health

Díaz

Reese

2021

anim microbiome

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“…This suggests that seeking to understand microbial functions at the putative primary site of fermentation through faecal samples may not be feasible. This is not to say that faecal samples are not useful, as previous gut microbiome research on captive [22] and wild wombats [23,24] have yielded insights into wombat digestion and ecology. Eisenhofer et al used faecal samples from both captive and wild SHNWs to show that captivity has a large in uence on the faecal microbiota of SHNWs.…”

Section: Discussionmentioning

confidence: 99%

“…Eisenhofer et al used faecal samples from both captive and wild SHNWs to show that captivity has a large in uence on the faecal microbiota of SHNWs. They were also able to identify population-speci c microbial signatures and found a correlation between habitat type (degraded vs. intact) and faecal microbiota composition in SHNWs [23]. Shiffman et al used shotgun metagenomic sequencing on faecal samples collected from a captive SHNW, and found numerous microbial genes involved in plant degradation and urea recycling [22].…”

Section: Discussionmentioning

confidence: 99%

“…Previous research measuring short chain fatty acids indicates that most plant fermentation occurs in the proximal colon of both wombat species rather than in other regions of the GI tract [6]. To date, gut microbiota research in wombats has focused on faecal samples obtained from captive [22] and wild wombats [23,24], with nothing known about how microbial communities are structured throughout the GI tract, and how representative faeces are to other GI regions.…”

Section: Introductionmentioning

confidence: 99%

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Microbial biogeography of the wombat gastrointestinal tract

Eisenhofer

D’Agnese

Taggart

et al. 2021

Preprint

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Most herbivorous mammals have symbiotic microbes living in their gastrointestinal tracts that help with harvesting energy from recalcitrant plant fibre. The bulk of research into these microorganisms has focused on samples collected from faeces, representing the distal region of the gastrointestinal (GI) tract. However, the GI tract in herbivorous mammals is typically long and complex, containing different regions with distinct physico-chemical properties that can structure resident microbial communities. In this study, we characterised the microbial biogeography of the GI tracts in individuals of two species of wombats.Using 16S rRNA gene sequencing, our results show that GI microbial communities of wombats are structured by GI region. For both the bare-nosed wombat (Vombatus ursinus) and the southern hairy-nosed wombat (Lasiorhinus latifrons), we observed a trend of increasing microbial diversity from stomach to distal colon. The microbial composition in the first proximal colon region was more similar between wombat species than the corresponding distal colon region in the same species. We found several microbial genera that were differentially abundant between the first proximal colon and distal colon regions. Surprisingly, only 99 (10.6%) and 204 (18.7%) amplicon sequence variants (ASVs) were shared between the first proximal colon region and the distal colon region for the bare-nosed and southern hairy-nosed wombat, respectively.These results suggest that microbial communities in the first proximal colon region—the putative site of primary plant fermentation in wombats—are distinct from the distal colon, and that faecal samples may have limitations in capturing the diversity of these communities. While faeces are still a valuable and effective means of characterising the distal colon microbiota, future work seeking to better understand how GI microbiota impact the energy economy of wombats (and potentially other hindgut-fermenting mammals) may need to take gut biogeography into account.

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Metagenomic analysis of marsupial gut microbiomes provides a genetic basis for the low methane economy

Bowerman,

Lu,

McRae

et al. 2024

Preprint

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The potent greenhouse gas methane is an end-product of plant biomass digestion by gut microbiota, though the amount produced and/or released varies among herbivorous animals. On a per unit of feed basis, macropodid marsupials (e.g. kangaroos) are widely thought to be low methane-emitting herbivores compared to high methane-producing ruminant livestock. How the gut microbiome contributes to the low methane status of marsupials is not well understood but of high potential value for a low methane economy. Here, we analyse the faecal metagenomes of 14 different marsupial species and 1,394 derived metagenome-assembled genomes (MAGs), focusing on the functional distinction of the bacterial and archaeal communities compared to ruminant faecal microbiomes. Though composition and function of the marsupial gut microbiome considerably varied across and within animal species, there was a clear host-associated bacterial signature for the community that differed significantly between marsupial hosts and compared to ruminants. Of particular note was a range of Bacteroidota, Campylobacterota, Desulfobacterota, Pseudomonadota and Verrucomicrobiota species that were enriched in marsupials and encode H2-uptake hydrogenases that mediate hydrogenotrophic respiration. Additionally, in support of an enrichment of electron sinks, enzymes for butyrate, propionate, and glutamate production, as well as nitrate, nitrite, and fumarate respiration were enriched in marsupials. Collectively, these data suggest that, by favouring an enrichment of alternate hydrogen sinks of bacterial origin, the low methane phenotype reported for marsupials is feasible and offers a genetic basis to pursue reductions of livestock methane emissions.

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Signatures of landscape and captivity in the gut microbiota of Southern Hairy-nosed Wombats (Lasiorhinus latifrons)

Cited by 13 publications

References 61 publications

Possibilities and limits for using the gut microbiome to improve captive animal health

Possibilities and limits for using the gut microbiome to improve captive animal health

Microbial biogeography of the wombat gastrointestinal tract

Metagenomic analysis of marsupial gut microbiomes provides a genetic basis for the low methane economy

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