Quinones are growth factors for the human gut microbiota

Fenn, Kathrin; Strandwitz, Philip; Stewart, Eric J.; Dimise, Eric J.; Rubin, Sarah; Gurubacharya, Shreya; Clardy, Jon; Lewis, Kim

doi:10.1186/s40168-017-0380-5

Cited by 84 publications

(73 citation statements)

References 36 publications

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“…A few attempts have been made to discover microbial interactions via signaling molecules that promote the growth of specific microbial types. Short peptides (57), siderophores (58) and quinones (59) have been identified as growth-promoting factors for microbial types that cannot grow independently.…”

Section: Discussionmentioning

confidence: 99%

Cultivatingin situtriggers growth of previously uncultivated microorganisms via a growth initiation factor in nature

Jung

Machida

Nakao

et al. 2019

Preprint

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Most microorganisms resist cultivation under standard laboratory conditions. On the other hand, to cultivate microbes in a membrane-bound device incubated in nature (in situcultivation) is an effective approach. In the present study, we appliedin situcultivation to isolate diverse previously uncultivated marine sponge-associated microbes and comparatively analyzed this method’s efficiencies with those of the conventional method. Then, we attempted to clarify the key and unknown mechanism ofin situcultivation by focusing on growth triggering via growth initiation factor. We hypothesized that majority of environmental microorganisms are in nongrowing state and requiring “growth initiation factor” for the recovery and that can be provided from environments. Consequently, significantly more novel and diverse microbial types were isolated viain situcultivation than by standard direct plating (SDP). Next, the effect of the sponge extract on starvation recovery was compared between strains derived fromin situand SDP cultivation. Adding small amounts of the sponge extracts to the medium elevated the colony-formation efficiencies of thein situstrains at the starvation recovery step, while it showed no positive effect on that of SDP strains. Conversely, specific growth rates or carrying capacities of all tested strains were not positively affected. These results indicate that, 1) the sponge extract contains chemical compounds that facilitate starvation recovery, these substances selectively worked on thein situstrains, and 2) growth initiation factor in the sponge extract did not continuously promote growth activity but worked as triggers for regrowth (resuscitation from dormancy).ImportanceMost microbial species resist cultivation under laboratory condition. This is critical impediment for both academic and applied microbiology, and thus clarification of the mechanism of microbial uncultivability is highly demanded. Several evidences have been reported that to cultivate microbes in a membrane-bound device incubated in nature (in situcultivation) is an effective approach. However, the mechanism behind this approach has not been clarified. The present study shows the evidence that 1) initiating growth is a key for cultivating previously uncultivated microbes rather than simple growth promotion, and 2) growth initiation factor (signaling-like compounds) in natural environments stimulate microbial resuscitation from a nongrowing state. Since no study has focused on growth initiation for cultivation of previously uncultivated microorganisms, the discovery shown in the present study provides a new insight into microorganisms previously considered uncultivable and a microbial growth controlling system in nature.

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Section: Discussionmentioning

confidence: 99%

Cultivatingin situtriggers growth of previously uncultivated microorganisms via a growth initiation factor in nature

Jung

Machida

Nakao

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…The PAB have been shown to affect the growth of a wide variety of microbes, including bacteria, yeasts and moulds. Most studies have focused on selectively inhibiting the growth of microbes (Holo et al, 2002;Lind et al, 2007;Schwenninger et al, 2008;Faye et al, 2011), but the PAB's properties of stimulating growth are also known (Kaneko, 1999;Jan et al, 2002;Warminska-Radyko et al, 2002); 1,4-dihydroxy-2-naphthoic acid secreted by PAB can stimulate the growth of Bifidobacteria and various other anaerobes (Kaneko, 1999;Fenn et al, 2017). In line with this, it was reported that P. acidipropionicii P169 could stimulate rumen feed degradation (Sanchez et al, 2014).…”

Section: Effects On Production Of Volatile Fatty Acids and Methanementioning

confidence: 93%

“…The PAB might stimulate the growth and activities of ruminal microorganisms by providing growth factors, e.g. 1,4-dihydroxy-2-naphthoic acid (Kaneko, 1999;Fenn et al, 2017).…”

Section: Feed Degradationmentioning

confidence: 99%

Propionic acid bacteria enhance ruminal feed degradation and reduce methane production in vitro

Chen

Harstad

McAllister

et al. 2020

Acta Agriculturae Scandinavica, Section A — Animal Science

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Thirty-one strains of propionic acid bacteria were screened for their effects on methane production and volatile fatty acid concentrations using in vitro assays of rumen fluid from Norwegian dairy cows and a grass silage-concentrate mixture as substrate. Nine of 31 strains were further analysed for effects on substrate degradation. Propionic acid bacteria led to reductions of up to 20% in methane production. Seven strains stimulated volatile fatty acid production, and in their presence in vitro substrate degradation tended to increase (P < .10). Most consistent results were found with Propionibacterium thoenii T159, which reduced methane production by 20% and caused 8% and 21% overall increases in substrate degradation and total volatile acid production, respectively (P < .05). Concomitant beneficial effects of a reduction in methane emissions and an increase in feed degradation suggest that this strain may be a promising tool for improving the productive performance of dairy cows.

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“…3, bottom panel). Similarly, Bilophila wadsworthia was previously recovered in mixed cultures, where growth depended on a "helper strain" producing essential growth-promoting factors (quinones) (39,42). Several bacteria can act as "helpers" supplying quinones, including E. lenta, Eubacterium rectale, and different Bacteroides species.…”

Section: Resultsmentioning

confidence: 99%

Planktonic and Sessile Artificial Colonic Microbiota Harbor Distinct Composition and Reestablish Differently upon Frozen and Freeze-Dried Long-Term Storage

et al. 2020

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Biofilm-associated, sessile communities represent the major bacterial lifestyle, whereas planktonic cells mainly appear during initial colonization of new surfaces. Previous research, mainly performed with pathogens, demonstrated increased environmental stress tolerance of biofilm-growing compared to planktonic bacteria. The lifestyle-specific stress response of colonic microbiota, both natural and fermentation produced, has not been addressed before. Planktonic and sessile “artificial” colonic microbiota delivered by PolyFermS continuous fermentation models can provide a controllable and reproducible alternative to fecal transplantation in treating gastrointestinal disorders. We therefore characterized planktonic and sessile microbiota produced in two PolyFermS models inoculated with immobilized fecal microbiota and comparatively tested their levels of tolerance of frozen storage (–80°C) and freeze-dried storage (4°C) for 9 months to mimic preservation strategies for therapeutic applications. Sessile microbiota harbored next to shared taxa a unique community distinguishable from planktonic microbiota. Synergistetes and Proteobacteria were highly represented in sessile microbiota, while Firmicutes were more abundant in planktonic microbiota. The community structure and metabolic activity of both microbiota, monitored during standardized reactivation batch fermentations, were better preserved after frozen storage than dried storage, indicated by higher Bray-Curtis similarity and enhanced recovery of metabolite production. For both lifestyles, reestablishment of Bacteroidaceae was impaired after frozen and dried storage along with reduced propionate formation. In contrast, butyrate production was maintained after reactivation despite compositional rearrangements within the butyrate-producing community. Unexpectedly, the rate of recovery of metabolite production was lower after preservation of sessile than planktonic microbiota. We speculate that higher functional dependencies between microbes might have led to the lower stress tolerance of sessile than planktonic microbiota. IMPORTANCE Fecal microbiota transplantation has been successfully applied in the treatment of recurrent Clostridium difficile infection and has been suggested as an alternative therapy for other intestinal disorders such as inflammatory bowel disease or metabolic syndrome. “Artificial” colonic microbiota delivered by PolyFermS continuous fermentation models can provide a controllable and reproducible alternative to fecal transplantation, but effective preservation strategies must be developed. In this study, we systematically investigated the response of sessile and planktonic artificial colonic microbiota to cryopreservation and lyophilization. We suggest that functional redundancy is an important factor in providing functional stability with respect to exposure to stress during processing and storage. Functional redundancy in compositionally reduced microbial systems may be considered when designing microbial products for therapy.

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Quinones are growth factors for the human gut microbiota

Cited by 84 publications

References 36 publications

Cultivatingin situtriggers growth of previously uncultivated microorganisms via a growth initiation factor in nature

Cultivatingin situtriggers growth of previously uncultivated microorganisms via a growth initiation factor in nature

Propionic acid bacteria enhance ruminal feed degradation and reduce methane production in vitro

Planktonic and Sessile Artificial Colonic Microbiota Harbor Distinct Composition and Reestablish Differently upon Frozen and Freeze-Dried Long-Term Storage

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