Implications of indoor microbial ecology and evolution on antibiotic resistance

Maamar, Sarah Ben; Hu, Jinglin; Hartmann, Erica M.

doi:10.1038/s41370-019-0171-0

Cited by 27 publications

(14 citation statements)

References 120 publications

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“…Although environmental acquisition may promote heterogeneity within and between hosts [44], its role rarely has been considered a differentiating factor between wild and captive hosts. Husbandry practices and veterinary care, for example, introduce cleaning products and antibiotics to the microbial environment of captive animals [45,46], further differentiating it from the 'native' environment [47], with potentially critical consequences to microbiome structure and function.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

Bornbusch

Greene

et al. 2022

anim microbiome

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Background Inter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia. Results The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota. Conclusions As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.

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Section: Introductionmentioning

confidence: 99%

Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

Bornbusch

Greene

et al. 2022

anim microbiome

View full text Add to dashboard Cite

show abstract

“…Although environmental acquisition may promote heterogeneity within and between hosts 43 , its role rarely has been considered a differentiating factor between wild and captive hosts. Husbandry practices and veterinary care, for example, introduce cleaning products and antibiotics to the microbial environment of captive animals 44,45 , further differentiating it from natural habitats 46 , with potentially critical consequences to microbiome structure and function.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota

Bornbusch

et al. 2021

Preprint

View full text Add to dashboard Cite

Background: Inter-population variation in host-associated microbiota reflects differences in the hosts' environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes - an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used source-sink ecological theory to examine covariation between the two types of consortia. Results: The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or condition. Variation in microbial composition was inconsistent with either a single, representative gut community for wild conspecifics or a universal 'signal of captivity' that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemurs within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities were most distinct between the two continents, and there was significant and context-specific covariation between lemur gut and soil microbiota. Conclusions: As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple 'captive vs. wild' dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.

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“…These findings provide insights into processes shaping the indoor microbiomes which will aid the development of effective strategies to control microbial exposure risks of occupants in educational facilities. spread of antibiotics resistance (Ben Maamar et al, 2020;Song et al, 2020), and particularly transmission of pathogens which is an urgent concern due to the rapid spread of severe acute respiratory syndrome coronavirus 2 (SARS-Cov-2) in indoor environments (Allen and Marr, 2020).…”

Section: G R a P H I C Abstract Abstractmentioning

confidence: 99%