Regulation of Gene Expression in a Mixed-Genus Community: Stabilized Arginine Biosynthesis inStreptococcus gordoniiby Coaggregation withActinomyces naeslundii

Abstract

Interactions involving genetically distinct bacteria, for example, between oral streptococci and actinomyces, are central to dental plaque development. A DNA microarray identified Streptococcus gordonii genes regulated in response to coaggregation with Actinomyces naeslundii. The expression of 23 genes changed >3-fold in coaggregates, including that of 9 genes involved in arginine biosynthesis and transport. The capacity of S. gordonii to synthesize arginine was assessed using a chemically defined growth medium. In monoculture, streptococcal arginine biosynthesis was inefficient and streptococci could not grow aerobically at low arginine concentrations. In dual-species cultures containing coaggregates, however, S. gordonii grew to high cell density at low arginine concentrations. Equivalent cocultures without coaggregates showed no growth until coaggregation was evident (9 h). An argH mutant was unable to grow at low arginine concentrations with or without A. naeslundii, indicating that arginine biosynthesis was essential for coaggregation-induced streptococcal growth. Using quantitative reverse transcriptase PCR, the expression of argC, argG, and pyrA b was strongly (10-to 100-fold) up-regulated in S. gordonii monocultures after 3 h of growth when exogenous arginine was depleted. Cocultures without induced coaggregation showed similar regulation. However, within 1 h after coaggregation with A. naeslundii, the expression of argC, argG, and pyrA b in S. gordonii was partially upregulated although arginine was plentiful, and mRNA levels did not increase further when arginine was diminished. Thus, A. naeslundii stabilizes S. gordonii expression of arginine biosynthesis genes in coaggregates but not cocultures and enables aerobic growth when exogenous arginine is limited.

Current understanding of multi‐species biofilms

“…Jakubovics et al have used DNA microarray to systematic search Streptococcus gordonii (S. gordonii) genes regulated in response to coaggregation with A. naeslundii in multi-species dental plague biofilm. In this study, they found that 9 S. gordonii genes involved in arginine biosynthesis and transport are highly induced in coaggregates, but not in co-cultures with A. naeslundii, which enables aerobic S. gordonii growth when exogenous arginine is limited [49]. Wen et al reported that expression of Streptococcus mutans (S. mutans) virulence genes is significantly reduced in multi-species biofilms with S. oralis or Lactobacillus casei [50].…”

Filifactor alocis: The Newly Discovered Kid on the Block with Special Talents

“…It is noteworthy that P. gingivalis and F. alocis interspecies interaction resulted in the up-regulation of arginine deiminase (HMPREF_0389_01584) and carbamate kinase (HMPREF_0389_00535) in F. alocis (unpublished observations). While it may use a novel arginine catabolic pathway compared with other AAGPRs in the periodontal pocket (Uematsu et al, 2003), its relative abundance in the periodontal pocket and its enhanced ability to produce ammonia could promote species co-habitation and survival (Jakubovics et al, 2008). Because butyrate is a metabolic end-product from arginine, it could likely also have an impact on other microbial interactions, including viruses, in the oral cavity.…”

Bacterial interactions in dental biofilm

“…In the presence of A. naeslundii, S. gordonii can grow under arginine depletion conditions in which S. gordonii usually does not survive. 93,94 Veillonella. Veillonella species can produce vitamin K, which can be utilized by Prevotella spp and Porphyromonas spp for their growth.…”