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Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species.

ABSTRACT: Mammalian chemosignals-or scent marks-are characterized by astounding chemical diversity, reflecting both complex biochemical pathways that produce them and rich information exchange with conspecifics. The microbiome of scent glands was thought to play prominent role in the chemical signal synthesis, with diverse microbiota metabolizing glandular products to produce odorants that may be used as chemosignals. Here, we use gas chromatography-mass spectrometry and metagenomic shotgun sequencing to explore this phenomenon in the anogenital gland secretions (AGS) of the giant panda (Ailuropoda melanoleuca). We find that this gland contains a diverse community of fermentative bacteria with enzymes that support metabolic pathways (e.g., lipid degradation) for the productions of volatile odorants specialized for chemical communication. We found quantitative and qualitative differences in the microbiota between AGS and digestive tract, a finding which was mirrored by differences among chemical compounds that could be used for olfactory communication. Volatile chemical compounds were more diverse and abundant in AGS than fecal samples, and our evidence suggests that metabolic pathways have been specialized for the synthesis of chemosignals for communication. The panda's microbiome is rich with genes coding for enzymes that participate in the fermentation pathways producing chemical compounds commonly deployed in mammalian chemosignals. These findings illuminate the poorly understood phenomena involved in the role of symbiotic bacteria in the production of chemosignals.

SUBMITTER: Zhou W

PROVIDER: S-EPMC8245644 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bacteria respond to stressful growth conditions through a conserved phenomenon of stringent response mediated by synthesis of stress alarmones ppGpp and pppGpp [referred to as (p)ppGpp]. (p)ppGpp synthesis is known to occur by ribosome-associated RelA. In addition, a dual-function protein, SpoT (with both synthetase and hydrolase activities), maintains (p)ppGpp homeostasis. The presence of (p)ppGpp is also known to contribute to antibiotic resistance in bacteria. Mycobacterium smegmatis possesses Arr, which inactivates rifampin by its ADP ribosylation. Arr has been shown to be upregulated in response to stress. However, the roles Arr might play during growth have remained unclear. We show that Arr confers growth fitness advantage to M. smegmatis even in the absence of rifampin. Arr deficiency in M. smegmatis resulted in deficiency of biofilm formation. Further, we show that while Arr does not interact with the wild-type Escherichia coli ribosomes, it interacts with them when the E. coli ribosomal protein L11 (a stringent response regulator) is replaced with its homolog from M. smegmatis The Arr interaction with E. coli ribosomes occurs even when the N-terminal 33 amino acids of its L11 protein were replaced with the corresponding sequence of M. smegmatis L11 (Msm-EcoL11 chimeric protein). Interestingly, Arr interaction with the E. coli ribosomes harboring M. smegmatis L11 or Msm-EcoL11 results in the synthesis of ppGpp in vivo Our study shows a novel role of antibiotic resistance gene arr in stress response.IMPORTANCEMycobacterium smegmatis, like many other bacteria, possesses an ADP-ribosyltransferase, Arr, which confers resistance to the first-line antituberculosis drug, rifampin, by its ADP ribosylation. In this report, we show that in addition to its known property of conferring resistance to rifampin, Arr confers growth fitness advantage to M. smegmatis even when there is no rifampin in the growth medium. We then show that Arr establishes species-specific interactions with ribosomes through the N-terminal sequence of ribosomal protein L11 (a stringent response regulator) and results in ppGpp (stress alarmone) synthesis. Deficiency of Arr in M. smegmatis results in deficiency of biofilm formation. Arr protein is physiologically important both in conferring antibiotic resistance as well as in mediating stringent response.

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Symbiotic bacteria mediate volatile chemical signal synthesis in a large solitary mammal species.

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