Respiration metabolism of Group B Streptococcus is activated by environmental haem and quinone and contributes to virulence

Abstract

SummaryGroup B Streptococcus (GBS) is a common constituent of the vaginal microflora, but its transmission to newborns can cause life-threatening sepsis, pneumonia and meningitis. Energy metabolism of this opportunist pathogen has been deduced to be strictly fermentative. We discovered that GBS undergoes respiration metabolism if its environment supplies two essential respiratory components: quinone and haem. Respiration metabolism led to significant changes in growth characteristics, including a doubling of biomass and an altered metabolite profile under the tested conditions. The GBS respiratory chain is inactivated by: (i) withdrawing haem and/or quinone, (ii) treating cultures with a respiration inhibitor or (iii) inactivating the cydA gene product, a subunit of cytochrome bd quinol oxidase, in all cases resulting in exclusively fermentative growth. cydA inactivation reduced GBS growth in human blood and strongly attenuated virulence in a neonatal rat sepsis model, suggesting that the animal host may supply the components that activate GBS respiration. These results suggest a role of respiration metabolism in GBS dissemination. Our findings show that environmental factors can increase the flexibility of GBS metabolism by activating a newly identified respiration chain. The need for two environmental factors may explain why GBS respiration metabolism was not found in previous studies.

Stress Physiology of Lactic Acid Bacteria

“…Inactivation of cydA negatively affected GBS growth in blood and strongly attenuated virulence in a neonatal rat sepsis model (517). The animal pathogen S. uberis also contains cytochrome bd oxidase; since it lacks quinone and heme biosynthesis pathways, it is thought to use a similar strategy to activate respiration.…”

“…The genome of GBS encodes a cytochrome bd oxidase (CydABCD), and the organism can engage in respiratory metabolism when the environment provides quinone and heme (517). Inactivation of cydA negatively affected GBS growth in blood and strongly attenuated virulence in a neonatal rat sepsis model (517).…”

Structural Basis for the Transcriptional Regulation of Heme Homeostasis in Lactococcus lactis

“…L. lactis undergoes a metabolic shift from fermentation to respiration in an aerobic environment when heme is supplied (11,12). Acquired heme is used as a source of heme, rather than of iron, to activate cytochrome oxidase (cytochrome bd) for oxygen respiration because this bacterium cannot biosynthesize heme (10,13,14).…”

Dynamic Stresses of Lactic Acid Bacteria Associated to Fermentation Processes

“…It was generally believed that these bacteria could under no condition use oxygen as the terminal electron acceptor [17]. However, many LAB have NADH oxidase and some can even express a functionally active respiratory chain in the presence of heme [51][52][53][54][55][56][57]. Respiration-competent LAB differ from the features of Escherichia coli and Bacillus subtilis, since they carry limited equipment for respiration.…”