Co-cultivation of Mortierellaceae with Pseudomonas helmanticensis affects both their growth and volatilome

Probst, Maraike; Telagathoti, Anusha; Siewert, Bianka; Khomenko, Iuliia; Betta, Emanuela; Biasioli, Franco; Peintner, Ursula

doi:10.1038/s41598-023-29134-6

Cited by 2 publications

(2 citation statements)

References 48 publications

(59 reference statements)

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“…1C ). These findings are consistent with those observed in studies of soil bacterial communities, where interspecies interactions have been found to either promote or constrain volatile production ( 51 ). It is therefore likely that oral polymicrobial communities exhibit enhanced or suppressed CH 3 SH production depending on interactions between the community members, which highlights the need for studies to resolve individual roles of different species.…”

Section: Discussionsupporting

confidence: 91%

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Hara,

Sakanaka,

Lamont

et al. 2024

mSystems

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The major oral odor compound methyl mercaptan (CH 3 SH) is strongly associated with halitosis and periodontitis. CH 3 SH production stems from the metabolism of polymicrobial communities in periodontal pockets and on the tongue dorsum. However, understanding of CH 3 SH-producing oral bacteria and their interactions is limited. This study aimed to investigate CH 3 SH production by major oral bacteria and the impact of interspecies interactions on its generation. Using a newly constructed large-volume anaerobic noncontact coculture system, Fusobacterium nucleatum was found to be a potent producer of CH 3 SH, with that production stimulated by metabolic interactions with Streptococcus gordonii , an early dental plaque colonizer. Furthermore, analysis of extracellular amino acids using an S. gordonii arginine-ornithine antiporter (ArcD) mutant demonstrated that ornithine excreted from S. gordonii is a key contributor to increased CH 3 SH production by F. nucleatum . Further study with 13 C, 15 N-methionine, as well as gene expression analysis, revealed that ornithine secreted by S. gordonii increased the demand for methionine through accelerated polyamine synthesis by F. nucleatum , leading to elevated methionine pathway activity and CH 3 SH production. Collectively, these findings suggest that interaction between S. gordonii and F. nucleatum plays a key role in CH 3 SH production, providing a new insight into the mechanism of CH 3 SH generation in oral microbial communities. A better understanding of the underlying interactions among oral bacteria involved in CH 3 SH generation can lead to the development of more appropriate prophylactic approaches to treat halitosis and periodontitis. An intervention approach like selectively disrupting this interspecies network could also offer a powerful therapeutic strategy. IMPORTANCE Halitosis can have a significant impact on the social life of affected individuals. Among oral odor compounds, CH 3 SH has a low olfactory threshold and halitosis is a result of its production. Recently, there has been a growing interest in the collective properties of oral polymicrobial communities, regarded as important for the development of oral diseases, which are shaped by physical and metabolic interactions among community participants. However, it has yet to be investigated whether interspecies interactions have an impact on the production of volatile compounds, leading to the development of halitosis. The present findings provide mechanistic insights indicating that ornithine, a metabolite excreted by Streptococcus gordonii , promotes polyamine synthesis by Fusobacterium nucleatum , resulting in a compensatory increase in demand for methionine, which results in elevated methionine pathway activity and CH 3 SH production. Elucidation of the mechanisms related to CH 3 SH production is expected to lead to the development of new strategies for managing halitosis.

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Section: Discussionsupporting

confidence: 91%

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Hara,

Sakanaka,

Lamont

et al. 2024

mSystems

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“…Pseudomonas spp. have been among the most commonly cited bacterial genera establishing inter-kingdom associations with fungi ( Probst et al., 2023 ), including in the context of co-infections ( Grainha et al., 2020 ; Santos-Fernandez et al., 2023 ). Pseudomonas spp.…”

Section: Discussionmentioning

confidence: 99%

Associated bacterial communities, confrontation studies, and comparative genomics reveal important interactions between Morchella with Pseudomonas spp.

Cailleau,

Hanson,

Cravero

et al. 2023

Front. Fungal Biol.

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Members of the fungal genus Morchella are widely known for their important ecological roles and significant economic value. In this study, we used amplicon and genome sequencing to characterize bacterial communities associated with sexual fruiting bodies from wild specimens, as well as vegetative mycelium and sclerotia obtained from Morchella isolates grown in vitro. These investigations included diverse representatives from both Elata and Esculenta Morchella clades. Unique bacterial community compositions were observed across the various structures examined, both within and across individual Morchella isolates or specimens. However, specific bacterial taxa were frequently detected in association with certain structures, providing support for an associated core bacterial community. Bacteria from the genus Pseudomonas and Ralstonia constituted the core bacterial associates of Morchella mycelia and sclerotia, while other genera (e.g., Pedobacter spp., Deviosa spp., and Bradyrhizobium spp.) constituted the core bacterial community of fruiting bodies. Furthermore, the importance of Pseudomonas as a key member of the bacteriome was supported by the isolation of several Pseudomonas strains from mycelia during in vitro cultivation. Four of the six mycelial-derived Pseudomonas isolates shared 16S rDNA sequence identity with amplicon sequences recovered directly from the examined fungal structures. Distinct interaction phenotypes (antagonistic or neutral) were observed in confrontation assays between these bacteria and various Morchella isolates. Genome sequences obtained from these Pseudomonas isolates revealed intriguing differences in gene content and annotated functions, specifically with respect to toxin-antitoxin systems, cell adhesion, chitinases, and insecticidal toxins. These genetic differences correlated with the interaction phenotypes. This study provides evidence that Pseudomonas spp. are frequently associated with Morchella and these associations may greatly impact fungal physiology.

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Co-cultivation of Mortierellaceae with Pseudomonas helmanticensis affects both their growth and volatilome

Cited by 2 publications

References 48 publications

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Interspecies metabolite transfer fuels the methionine metabolism of Fusobacterium nucleatum to stimulate volatile methyl mercaptan production

Associated bacterial communities, confrontation studies, and comparative genomics reveal important interactions between Morchella with Pseudomonas spp.

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