Impaired respiration elicits SrrAB-dependent programmed cell lysis and biofilm formation in Staphylococcus aureus

Mashruwala, Ameya A.; Guchte, Adriana van de; Boyd, Jeffrey M.

doi:10.7554/elife.23845

Cited by 103 publications

(106 citation statements)

References 117 publications

Supporting

Mentioning

103

Contrasting

Order By: Relevance

“…However, the mechanisms underlying the influence of oxygen upon biofilm formation have yet to be fully described. We recently reported that oxygen impacts S. aureus biofilm formation in its capacity as a terminal electron acceptor for cellular respiration (21). Decreased oxygen concentrations lead to diminished respiration, which serves as a signal that elicits programmed cell lysis (PCL), culminating in increased biofilm formation (21).…”

mentioning

confidence: 99%

“…We recently reported that oxygen impacts S. aureus biofilm formation in its capacity as a terminal electron acceptor for cellular respiration (21). Decreased oxygen concentrations lead to diminished respiration, which serves as a signal that elicits programmed cell lysis (PCL), culminating in increased biofilm formation (21). Chemical or physiological conditions that diminish respiration prompt increased biofilm formation.…”

mentioning

confidence: 99%

“…Likewise, heme (hemB::Tn) or menaquinone (menF::Tn) auxotrophs that are incapable of respiration form increased biofilms aerobically. PCL occurs via increased expression of a peptidoglycan hydrolase (AtlA) and decreased expression of the AtlA-inhibiting cell surface glycopolymer wall teichoic acid (WTA) (21). Increased AltA activity results in the release of high-molecularweight DNA and cytosolic proteins into the extracellular milieu.…”

mentioning

confidence: 99%

“…Increased AltA activity results in the release of high-molecularweight DNA and cytosolic proteins into the extracellular milieu. The DNA and proteins that are released are incorporated into the biofilm matrix and serve as integral structural elements (21).…”

mentioning

confidence: 99%

“…The phosphorylated RR binds to target DNA sequences and regulates transcription, resulting in a tailored physiological response. PCL and fermentative biofilm formation are governed, in part, by the SrrAB TCRS and occur in response to the accumulation of reduced menaquinone (21). SrrAB-dependent biofilm formation is silenced in the absence of menaquinone; however, a menF::Tn strain still forms increased biofilms in the presence of oxygen by an undefined mechanism (21).…”

mentioning

confidence: 99%

See 4 more Smart Citations

SaeRS Is Responsive to Cellular Respiratory Status and Regulates Fermentative Biofilm Formation in Staphylococcus aureus

et al. 2017

Self Cite

View full text Add to dashboard Cite

Biofilms are multicellular communities of microorganisms living as a quorum rather than as individual cells. The bacterial human pathogen Staphylococcus aureus uses oxygen as a terminal electron acceptor during respiration. Infected human tissues are hypoxic or anoxic. We recently reported that impaired respiration elicits a programmed cell lysis (PCL) phenomenon in S. aureus leading to the release of cellular polymers that are utilized to form biofilms. PCL is dependent upon the AtlA murein hydrolase and is regulated, in part, by the SrrAB two-component regulatory system (TCRS). In the current study, we report that the SaeRS TCRS also governs fermentative biofilm formation by positively influencing AtlA activity. The SaeRSmodulated factor fibronectin-binding protein A (FnBPA) also contributed to the fermentative biofilm formation phenotype. SaeRS-dependent biofilm formation occurred in response to changes in cellular respiratory status. Genetic evidence presented suggests that a high cellular titer of phosphorylated SaeR is required for biofilm formation. Epistasis analyses found that SaeRS and SrrAB influence biofilm formation independently of one another. Analyses using a mouse model of orthopedic implant-associated biofilm formation found that both SaeRS and SrrAB govern host colonization. Of these two TCRSs, SrrAB was the dominant system driving biofilm formation in vivo. We propose a model wherein impaired cellular respiration stimulates SaeRS via an as yet undefined signal molecule(s), resulting in increasing expression of AtlA and FnBPA and biofilm formation.

show abstract

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations