Corynebacterium matruchotii fitness enhancement of adjacent streptococci by multiple mechanisms

Abstract

Polymicrobial biofilms are present in many environments particularly in the human oral cavity where they can prevent or facilitate the onset of disease. While recent advances have provided a clear picture of both the constituents and their biogeographical arrangement, it is still unclear what mechanisms of interaction occur between individual species in close proximity within these communities. In this study we investigated two mechanisms of interaction between the highly abundant supragingival plaque (SUPP) commensal Corynebacterium matruchotii and Streptococcus mitis which are directly adjacent in vivo. We discovered that C. matruchotii enhanced the fitness of streptococci dependent on its ability to detoxify streptococcal-produced hydrogen peroxide and its ability to oxidize lactate also produced by streptococci. We demonstrate that the fitness of adjacent streptococci was linked to that of C. matruchotii and that these mechanisms support the previously described “corncob” arrangement between these species but that this is favorable only in aerobic conditions. Further we utilized scanning electrochemical microscopy (SECM) to quantify lactate production and consumption between individual bacterial cells for the 1st time, revealing that lactate oxidation provides a fitness benefit to S. mitis and not pH mitigation. This study describes mechanistic interactions between two highly abundant human commensals that can explain their observed in vivo spatial arrangements and suggest a way by which they may help preserve a healthy oral bacterial community.

Mechanistic Assessment of Metabolic Interaction between Single Oral Commensal Cells by Scanning Electrochemical Microscopy

“…mitis and simultaneously oxidized by C. matruchotii in situ, thereby visually confirming previously hypothesized metabolite exchange at the single-cell level and supporting their observed in vivo spatial organization. Using finite element analysis, the mechanistic interaction between coculture was quantitatively assessed at the single-cell level as well.…”

“…This good agreement between the theoretical prediction and experimental currents validates the lactate consumption rate of C. matruchotii as k c,f ≥ 5 × 10 6 s –1 with thermodynamically favorable lactate oxidation under aerobic conditions, , i.e., an equilibrium constant, K eq = k c,f / k c,b ≥ 10 20 assumed in the theoretical simulation ( eq ). The simulated concentration profile of lactate near C.…”

“…Bacteria were grown overnight in BHI-YE and then washed by centrifugation in a defined medium, which is an amended version of Teknova EZ RICH (Teknova, M2105). The medium was prepared as described in the manufacturer’s instructions with the addition of vitamin solution, lipoic acid, folic acid, riboflavin, NAD + , and nucleotides at final concentrations from that of a chemically defined medium previously described and glucose at 10 mM. Bacteria were grown to an OD 600 of 0.3–0.5 and then diluted to final concentrations of 1.2 × 10 7 and 6.0 × 10 6 cfu of C.…”

“…matruchotii responds to S. mitis H 2 O 2 -dependent stress as well as lactate production . While the spatial organization/biogeography of these species has been well described, the exact nature of molecular interactions between these species, especially between individual cells, is relatively unknown.…”

A Brief Review of In Situ and Operando Electrochemical Analysis of Bacteria by Scanning Probes

“…FcMeOH [58] The pH of biocementation induced by Sporosarcina pasteurii Brine solution and urea [59] Biofilm formation of Shewanella oneidensis Ru(NH 3 ) 6 Cl 3 [60] Bacteria contamination in contact lenses, including Escherichia coli, Diphtheroid, Pseudomonas aeruginosa, Staphylococcus aureus, Fusobacterium nucleatum, Unidentified Gram(+) Bacilli Phosphate-buffered saline (PBS), FcMeOH [18] In addition to basic SECM, SECM combined with other techniques, such as AFM, inverted optical microscope, automatic motion control system, constant temperature chamber, SICM, or even fluorescence microscopy, has been developed. These advances will be discussed in the final part of this article.…”