Sharing of Moonlighting Proteins Mediates the Symbiotic Relationship among Intestinal Commensals

Nishiyama, Keita; Yong, Cheng-Chung; Moritoki, Nobuko; Kitazawa, Hideaki; Odamaki, Toshitaka; Xiao, Jin‐zhong; Mukai, T.

doi:10.1128/aem.02190-22

Cited by 4 publications

(1 citation statement)

References 68 publications

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“…UCYN-A also encodes its own EF-Tu, which was also highly abundant in the UCYN-A proteome. Bacterial EF-Tu proteins are known to be shared between different species ( 46 ) and to bind proteins of their symbiotic partners ( 47 ). This protein in UCYN-A likely mediates interactions with the surrounding B. bigelowii cell (Fig.…”

Section: Ucyn-a Imports B Bigelowii Nuclear-encoded Proteinsmentioning

confidence: 99%

Nitrogen-fixing organelle in a marine alga

Coale,

Loconte,

Turk-Kubo

et al. 2024

Science

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Symbiotic interactions were key to the evolution of chloroplast and mitochondria organelles, which mediate carbon and energy metabolism in eukaryotes. Biological nitrogen fixation, the reduction of abundant atmospheric nitrogen gas (N 2 ) to biologically available ammonia, is a key metabolic process performed exclusively by prokaryotes. Candidatus Atelocyanobacterium thalassa, or UCYN-A, is a metabolically streamlined N 2 -fixing cyanobacterium previously reported to be an endosymbiont of a marine unicellular alga. Here we show that UCYN-A has been tightly integrated into algal cell architecture and organellar division and that it imports proteins encoded by the algal genome. These are characteristics of organelles and show that UCYN-A has evolved beyond endosymbiosis and functions as an early evolutionary stage N 2 -fixing organelle, or “nitroplast.”

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Section: Ucyn-a Imports B Bigelowii Nuclear-encoded Proteinsmentioning

confidence: 99%

Nitrogen-fixing organelle in a marine alga

Coale,

Loconte,

Turk-Kubo

et al. 2024

Science

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Identification of moonlighting adhesins of highly-adhesive Lactobacillus plantarum PO23 isolated from the intestine of Paralichthys olivaceus

Liu,

Wang,

Wang

et al. 2024

Aquaculture

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Exploring strain-level diversity in the gut microbiome through mucin particle adhesion

Nishiyama,

Murakami,

Nakahata

et al. 2024

Appl Environ Microbiol

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Mucin glycoproteins are a significant source of carbon for the gut bacteria. Various gut microbial species possess diverse hydrolytic enzymes and catabolic pathways for breaking down mucin glycans, resulting in competition for the limited nutrients within the gut environment. Adherence to mucin glycans represents a crucial strategy used by gut microbes to access nutrient reservoirs. Understanding these properties is pivotal for comprehending the survival mechanisms of bacteria in the gastrointestinal tract. However, characterization of individual strains within the vast array of coexisting bacteria in the microbiome is challenging. To investigate this, we developed mucin-immobilized particles by immobilizing porcine gastric mucin (PGM) onto glass beads chemically modified with boronic acid. These PGM-immobilized particles were then anaerobically cultured with human fecal microbiota, and the bacteria adhering to PGM were isolated. Interestingly, the microbiome composition remained largely unchanged irrespective of PGM immobilization. Nonetheless, bacteria isolated from PGM-immobilized glass particles exhibited notably higher N -acetylgalactosaminidase activity compared to the control beads. Furthermore, Bacteroides strains isolated from PGM-immobilized glass particles displayed enhanced adhesive and metabolic properties to PGM. These findings underscore the utility of PGM particles in enriching and isolating specific microbes. Moreover, they highlight substantial differences in microbial properties at the strain level. We anticipate that PGM-immobilized particles will advance culture-based microbiome research, emphasizing the significance of strain-level characterization. IMPORTANCE Metabolism of mucin glycans by gut bacteria represents a crucial strategy for accessing nutrient reservoirs. The efficacy of mucin glycan utilization among gut bacteria hinges on the metabolic capabilities of individual strains, necessitating meticulous strain-level characterization. In this investigation, we used glass beads chemically immobilized with mucins to selectively enrich bacteria from fecal fermentation cultures, based on their superior adhesion to and metabolism of mucin glycoproteins. These findings lend support to the hypothesis that the physical interactions between bacteria and mucin glycoprotein components directly correlate with their capacity to utilize mucins as nutrient sources. Furthermore, our study implies that physical proximity may significantly influence bacterial nutrient acquisition within the ecosystem, facilitating gut bacteria’s access to carbohydrate components.

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Sharing of Moonlighting Proteins Mediates the Symbiotic Relationship among Intestinal Commensals

Abstract: The adhesion of intestinal bacteria to the mucus layer is an important colonization strategy in the gut environment. Generally, the bacterial adhesion process is a characteristic feature of the individual cell surface-associated adhesion factors secreted by a particular bacterium.

Cited by 4 publications

References 68 publications

Nitrogen-fixing organelle in a marine alga

Nitrogen-fixing organelle in a marine alga

Identification of moonlighting adhesins of highly-adhesive Lactobacillus plantarum PO23 isolated from the intestine of Paralichthys olivaceus

Exploring strain-level diversity in the gut microbiome through mucin particle adhesion

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