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Article

Ionizing Radiation Dose Differentially Affects the Host–Microbe Relationship over Time

1
Medical Readiness Systems Biology, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USA
2
The Geneva Foundation, Walter Reed Army Institute of Research, Silver Spring, MD 20910, USA
3
Armed Forces Radiobiology Research Institute, Uniformed Services University of the Health Sciences (USUHS), Bethesda, MD 20889, USA
*
Authors to whom correspondence should be addressed.
These authors contributed equally to this work.
Microorganisms 2024, 12(10), 1995; https://doi.org/10.3390/microorganisms12101995 (registering DOI)
Submission received: 13 August 2024 / Revised: 5 September 2024 / Accepted: 24 September 2024 / Published: 30 September 2024
(This article belongs to the Section Microbiomes)

Abstract

Microorganisms that colonize in or on a host play significant roles in regulating the host’s immunological fitness and bioenergy production, thus controlling the host’s stress responses. Radiation elicits a pro-inflammatory and bioenergy-expensive state, which could influence the gut microbial compositions and, therefore, the host–microbe bidirectional relationship. To test this hypothesis, young adult mice were exposed to total body irradiation (TBI) at doses of 9.5 Gy and 11 Gy, respectively. The irradiated mice were euthanized on days 1, 3, and 9 post TBI, and their descending colon contents (DCCs) were collected. The 16S ribosomal RNAs from the DCCs were screened to find the differentially enriched bacterial taxa due to TBI. Subsequently, these data were analyzed to identify the metagenome-specific biofunctions. The bacterial community of the DCCs showed increased levels of diversity as time progressed following TBI. The abundance profile was the most divergent at day 9 post 11 Gy TBI. For instance, an anti-inflammatory and energy-harvesting bacterium, namely, Firmicutes, became highly abundant and co-expressed in the DCC with pro-inflammatory Deferribacteres at day 9 post 11 Gy TBI. A systems evaluation found a diverging trend in the regulation profiles of the functional networks that were linked to the bacteria and metabolites of the DCCs, respectively. Additionally, the network clusters associated with lipid metabolism and bioenergy synthesis were found to be activated in the DCC bacteria but inhibited in the metabolite space at day 9 post 11 Gy. Taking these results together, the present analysis indicated a disrupted mouse–bacteria symbiotic relationship as time progressed after lethal irradiation. This information can help develop precise interventions to ameliorate the symptoms triggered by TBI.
Keywords: total body irradiation; fecal microbiome; fecal metabolite; host–microbiome association; 16S rRNA gene sequencing; functional metagenome; descending colon contents total body irradiation; fecal microbiome; fecal metabolite; host–microbiome association; 16S rRNA gene sequencing; functional metagenome; descending colon contents

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MDPI and ACS Style

Chakraborty, N.; Hoke, A.; Campbell, R.; Holmes-Hampton, G.; Kumar, V.P.; Moyler, C.; Gautam, A.; Hammamieh, R.; Ghosh, S.P. Ionizing Radiation Dose Differentially Affects the Host–Microbe Relationship over Time. Microorganisms 2024, 12, 1995. https://doi.org/10.3390/microorganisms12101995

AMA Style

Chakraborty N, Hoke A, Campbell R, Holmes-Hampton G, Kumar VP, Moyler C, Gautam A, Hammamieh R, Ghosh SP. Ionizing Radiation Dose Differentially Affects the Host–Microbe Relationship over Time. Microorganisms. 2024; 12(10):1995. https://doi.org/10.3390/microorganisms12101995

Chicago/Turabian Style

Chakraborty, Nabarun, Allison Hoke, Ross Campbell, Gregory Holmes-Hampton, Vidya P. Kumar, Candace Moyler, Aarti Gautam, Rasha Hammamieh, and Sanchita P. Ghosh. 2024. "Ionizing Radiation Dose Differentially Affects the Host–Microbe Relationship over Time" Microorganisms 12, no. 10: 1995. https://doi.org/10.3390/microorganisms12101995

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