Polymicrobial Aggregates in Human Saliva Build the Oral Biofilm

Simón-Soro, Áurea; Ren, Zhi; Krom, Bastiaan P.; Hoogenkamp, Michel A.; Cabello‐Yeves, Pedro J.; Daniel, Scott G.; Bittinger, Kyle; Tomás, Inmaculada; Koo, Hyun; Mira, Álex

doi:10.1128/mbio.00131-22

Cited by 35 publications

(33 citation statements)

References 48 publications

(79 reference statements)

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“…Taking the 16S rRNA metabarcoding and the metatranscriptomic analysis into account, we suggest that P. micra could arrive to the gut accompanied by other oral pathobionts, such as Fusobacterium, through the formation of polymicrobial aggregates. Micro-communities of bacteria are naturally found in human saliva and are composed by both aerobe and anaerobe microbes [107][108][109]. These bacterial aggregates appear to be able to grow and form bio lms more e ciently than if they travel as individual sessile cells [109].…”

Section: Discussionmentioning

confidence: 99%

“…Micro-communities of bacteria are naturally found in human saliva and are composed by both aerobe and anaerobe microbes [107][108][109]. These bacterial aggregates appear to be able to grow and form bio lms more e ciently than if they travel as individual sessile cells [109]. Metabolic interactions and co-operation between different genera could increase survival of fastidious bacteria, such as P. micra, during these translocation processes [107,108].…”

Section: Discussionmentioning

confidence: 99%

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Evidence for translocation of oral Parvimonas micra from the subgingival sulcus of the human oral cavity to the colorectal adenocarcinoma

Conde‐Pérez

Buetas

Aja‐Macaya

et al. 2022

Preprint

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Background: The carcinogenesis of colorectal cancer (CRC) is a multifactorial process involving both environmental and host factors, such as human genetics or the gut microbiome, which in CRC patients appears to be enriched in oral microorganisms. The aim of this work was to investigate the presence and activity of Parvimonas micrain CRC patients. To do that, samples collected from subgingival sulcus and neoplastic lesions were used for culturomics. Then, samples from different body locations (saliva, gingival crevicular fluid, feces, non-neoplastic colon mucosa, transition colon mucosa, adenocarcinoma, adenomas, metastatic and non-neoplastic liver samples) were used for 16S rRNA metabarcoding and metatranscriptomics. Whole genome sequencing was conducted for all P. micrastrains obtained. Results: Several P. micraisolates from the oral cavity and adenocarcinoma tissue from CRC patients were obtained. The comparison of oral and tumoral P. micra genomes identified that a pair of clones (PM89KC) were 99.2% identical between locations in one CRC patient, suggesting that the same clone migrated from oral cavity to the gut. The 16S rRNA metabarcoding analysis of samples from this patient revealed that P. micra cohabits with other periodontal pathogens such as Fusobacterium, Prevotella or Dialister, both in the intestine, liver and the subgingival space, which suggests that bacterial translocation from the subgingival environment to the colon or liver could be more efficient if these microorganisms travel together forming a synergistic consortium. In this way, bacteria might be able to perform tasks that are impossible for single cells. In fact, RNA-seq of the adenocarcinoma tissue confirmed the activity of these bacteria in the neoplastic tissue samples and revealed that different oral species, including P. micra, were significantly more active in the tumor compared to non-neoplastic tissue from the same individuals. Conclusion: P. micra appears to be able to translocate from the subgingival sulcus to the gut, where oral bacteria adapt to the new niche and could have a relevant role in carcinogenesis. According to our findings, periodontal disease, which increases the levels of these pathogens and facilitates their dissemination, could represent a risk factor for CRC development and P. micra could be used as a non-invasive CRC biomarker.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Evidence for translocation of oral Parvimonas micra from the subgingival sulcus of the human oral cavity to the colorectal adenocarcinoma

Conde‐Pérez

Buetas

Aja‐Macaya

et al. 2022

Preprint

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“…The implications of aging-associated collagen changes on oral bacterial invasion and translocation to other organs remains to be explored. Also, additional studies should explore the possible effect of other relevant collagen AGEs – such as pentosidine – on bacterial adhesion and early-biofilm progression, as well as their potential impact on surface colonization by bacterial aggregates in the oral cavity in the context of health and disease (Simon-Soro et al 2022).…”

Section: Discussionmentioning

confidence: 99%

Nanoscale dynamics of streptococcal adhesion to AGE-modified collagen

Leiva-Sabadini

Tiozzo-Lyon

Rivas

et al. 2022

Preprint

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The adhesion of initial colonizers such as Streptococcus mutans to collagen is critical for dentinal and root caries progression. One of the most described pathological and aging-associated changes in collagen, including dentinal collagen, is the generation of advanced glycation end-products (AGEs) such as methylglyoxal (MGO)-derived AGEs. Despite previous reports suggesting that AGEs alter bacterial adhesion to collagen, the biophysics driving oral streptococcal attachment to MGO-modified collagen remains largely understudied. Thus, the aim of this work was to unravel the dynamics of the initial adhesion of S. mutans to type-I collagen in the presence and absence of MGO-derived AGEs, by employing bacterial cell force-spectroscopy with atomic force microscopy (AFM). Type-I collagen gels were treated with 10mM MGO to induce AGE formation, which was characterized with microscopy and ELISA. Subsequently, AFM cantilevers were functionalized with living S. mutans UA 159 or S. sanguinis SK 36 cells and probed against collagen surfaces to obtain force-curves displaying bacterial attachment in real-time, from which the adhesion force, number of events, Poisson analysis, and contour and rupture lengths for each individual detachment event were computed. Furthermore, in-silico docking studies between the relevant S. mutans UA 159 collagen-binding protein SpaP and collagen were computed, in the presence and absence of MGO. Overall, results showed that MGO modification increased both the number and adhesion force of single-unbinding events between S. mutans and collagen, without altering the contour or rupture lengths. Both experimental and in-silico simulations suggest that this effect is due to increased specific and non-specific forces and interactions between S. mutans UA 159 and MGO-modified collagen substrates. In summary, these results suggest that collagen alterations due to glycation and AGE formation may play a role in early bacterial adherence to oral tissues, associated with conditions such as aging or chronic hyperglycemia, amongst others.

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“…This micron-scale patterning resulted in the protection of the oral pathogen Streptococcus mutans by surrounding oral commensals. In another example, to understand how oral microbes disperse and initiate biofilm formation, Simon-Soro et al combined microscopy with sequencing, showing that most of the microbial biomass in saliva is composed of aggregates containing a mix of both early and late colonizers ( 48 ). These diverse aggregates, not single cells, seeded the vast majority of biofilm formation in an in vitro model of the tooth surface.…”

Section: Current and Future Perspectivesmentioning

confidence: 99%

Polymicrobial Interactions of Oral Microbiota: a Historical Review and Current Perspective

Zhang

Whiteley

Lewin

2022

mBio

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The oral microbiota is enormously diverse, with over 700 microbial species identified across individuals that play a vital role in the health of our mouth and our overall well-being. In addition, as oral diseases such as caries (cavities) and periodontitis (gum disease) are mediated through interspecies microbial interactions, this community serves as an important model system to study the complexity and dynamics of polymicrobial interactions.

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Polymicrobial Aggregates in Human Saliva Build the Oral Biofilm

Abstract: Microbes in biological fluids can be found as aggregates. How these multicellular structures bind to surfaces and initiate the biofilm life cycle remains understudied.

Cited by 35 publications

References 48 publications

Evidence for translocation of oral Parvimonas micra from the subgingival sulcus of the human oral cavity to the colorectal adenocarcinoma

Evidence for translocation of oral Parvimonas micra from the subgingival sulcus of the human oral cavity to the colorectal adenocarcinoma

Nanoscale dynamics of streptococcal adhesion to AGE-modified collagen

Polymicrobial Interactions of Oral Microbiota: a Historical Review and Current Perspective

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