Adaptation beyond the Stress Response: Cell Structure Dynamics and Population Heterogeneity in Staphylococcus aureus

Morikawa, Kazuya; Ohta, Toshiko; Tanaka, Yoshikazu; Msadek, Tarek

doi:10.1264/jsme2.me10116

Cited by 17 publications

(16 citation statements)

References 87 publications

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“…A subset of organisms within many bacterial populations can be part of the normal growth cycle (Lechner et al, 2012), and this is certainly true for S. aureus SCVs, which are part of the normal growth cycle that occurs without any external stresses (Massey et al, 2001; Edwards, 2012). However, persisters also form as a response to harsh conditions such as antibiotics, acid, and starvation stresses (Morikawa et al, 2010). Biofilm formation can be thought of as a persister strategy (Abdallah et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Staphylococcus aureus Small Colony Variants (SCVs): a road map for the metabolic pathways involved in persistent infections

Proctor¹,

Kriegeskorte²,

Kahl³

et al. 2014

Front. Cell. Infect. Microbiol.

193

172

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Persistent and relapsing infections, despite apparently adequate antibiotic therapy, occur frequently with many pathogens, but it is an especially prominent problem with Staphylococcus aureus infections. For the purposes of this review, persistence will encompass both of the concepts of long term survival within the host, including colonization, and the concept of resisting antibiotic therapy even when susceptible in the clinical microbiology laboratory. Over the past two decades, the mechanisms whereby bacteria achieve persistence are slowly being unraveled. S. aureus small colony variants (SCVs) are linked to chronic, recurrent, and antibiotic-resistant infections, and the study of SCVs has contributed significantly to understanding of persistence. In our earlier work, defects in electron transport and thymidylate biosynthesis were linked to the development of the SCV phenotype (reviewed in 2006), thus this work will be discussed only briefly. Since 2006, it has been found that persistent organisms including SCVs are part of the normal life cycle of bacteria, and often they arise in response to harsh conditions, e.g., antibiotics, starvation, host cationic peptides. Many of the changes found in these early SCVs have provided a map for the discovery mechanisms (pathways) for the development of persistent organisms. For example, changes in RNA processing, stringent response, toxin-antitoxin, ribosome protein L6 (RplF), and cold shock protein B (CspB) found in SCVs are also found in other persisters. In addition, many classic persister organisms also show slow growth, hence SCVs. Recent work on S. aureus USA300 has elucidated the impact of aerobic expression of arginine deiminase genes on its ability to chronically colonize the skin and survive in abscesses. S. aureus SCVs also express arginine deiminase genes aerobically as well. Thus, many pathways found activated in electron transport type of SCVs are also increased in persisters that have intact electron transport. Many of these changes in metabolism result in slow growth; hence, small colonies are formed. Another common theme is that slow growth is also associated with reduced expression of virulence factors and enhanced uptake/survival within host cells. These adaptations to survive within the host are rooted in responses that were required for organisms to survive in a harsh environment long before they were mammals on the earth.

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Section: Introductionmentioning

confidence: 99%

Staphylococcus aureus Small Colony Variants (SCVs): a road map for the metabolic pathways involved in persistent infections

Proctor¹,

Kriegeskorte²,

Kahl³

et al. 2014

Front. Cell. Infect. Microbiol.

193

172

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“…It can be deducted from the above results that HSL4 strain resembled very closely to Staphylococcus lentus on the basis 16S rRNA sequence. However, HSL4 strain was quite distinct from Staphylococcus lentus on the basis of physiology and biochemical characteristics, therefore rendering HSL4 a different strain of Staphylococci genus having more diverse range for growth as described for other strains of Staphylococci (Graham and Wilkinson, 1992;Morikawa et al, 2010).…”

Section: Discussionmentioning

confidence: 95%

Physiological, Biochemical and Phylogenetic Characterization of Extremely Halophilic Bacteria Isolated From Khewra Mine, Pakistan

Leena¹

2018

Appl. Ecol. Env. Res.

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Leena et al.: Physiological, biochemical Abstract. Microflora entrapped in the salt deposits of Khewra salt mine, Pakistan has adapted to extreme conditions and nutrient scarcity to survive. Due to assumption that halophilic archaea dominate hypersaline environments, bacteria have often remained unexplored. The reports on extremely halophilic bacteria indigenous to Khewra mine are quite limited resulting in largely unexplored biodiversity of the salt mine. Here we attempted to fill that gap by isolating eight halophilic bacteria, out of which four extremely halophilic bacteria were selected for physiological, biochemical and molecular characterization. The phylogenetic characterization inferred through comparative partial 16S rRNA sequences identified these strains as HSL1-Oceanobacillus onchorhynci subsp. Incaldanensis, HSL4-Staphylococcus lentus, HSL6-Bacillus endophyticus and HSL7-Bacillus aquimaris. These isolates could tolerate a wide range of temperatures (15-45°C), pH (5-9) and survived up to 16% NaCl concentration. This tolerance is due to the stability of their enzymes. Enzyme assays revealed a substantial amount of production of protease, amylase, lipase, xylanase, urease, gelatinase, cellulose, and DNase. Conclusively, isolation and characterization of the extremely halophilic bacteria from Khewra mine indicated their important ecological role and contribution towards the microbial diversity. The ability to produce extreme-enzymes also established the potential of the isolates as valuable resources for significant biotechnological applications.

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“…Staphylococcus aureus cells responded to the osmotic challenge under limited growth conditions by displaying substantial alterations in amino acid and protein composition in the cytoplasm. Alterations in metabolic homeostasis may have resulted from a selection process, whereby exposure to the higher levels of NaCl selected for the proliferation of more favorable phenotypes originally present in the starter population of washed cells (Abu‐Qatouseh et al, ; Morikawa et al, ; von Eiff, ). However, there was no evidence of cell proliferation observed in the control cultures and nor was there any evidence of a decline of cell numbers in the NaCl treatments.…”

Section: Discussionmentioning

confidence: 99%

Amino acids and proteomic acclimation of Staphylococcus aureus when incubated in a defined minimal medium supplemented with 5% sodium chloride

et al. 2019

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Staphylococcus aureus is a versatile bacterium that can adapt to survive and grow in a wide range of salt concentrations. This study investigated whether the cells could mount a response to survive a challenge of 5% NaCl in a minimal incubation medium that would not support cell replication. Cells were grown in liquid culture, washed and then incubated for 90 min at 37°C in a medium that contained only glycine and glucose as substrates in PBS plus trace elements. The control cells were compared with a treatment group which was incubated with an additional 5% NaCl. Significantly more glycine was taken up by the cells exposed to 5% NaCl compared with control cells, and both groups consumed 99% of the glucose supplied. The NaCl treated cells had significantly higher cytoplasmic levels of proline and glutamic acid as well as lower levels of alanine and methionine compared with the controls ( p < 0.05). The levels of the two major cytoplasmic amino acids, aspartic acid and glycine, remained constant in control and treated cells. Proteomic analyses revealed that 10 proteins showed differential responses between the control and treatment groups. The reductions in proteins were primarily associated with processes of protein biosynthesis, pathogenicity, and cell adhesion. Since cell numbers remained constant during the incubation period in minimal medium, it was concluded that there was no cell division to support population growth. The results provided evidence that the cells in the minimal medium exposed to the NaCl treatment underwent in situ homeostatic changes to adjust to the new environmental conditions. It was proposed that this represented a phenotypic shift to form cells akin to small colony variants, with lower metabolic rates and lower levels of key proteins associated with pathogenicity.

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Adaptation beyond the Stress Response: Cell Structure Dynamics and Population Heterogeneity in Staphylococcus aureus

Cited by 17 publications

References 87 publications

Staphylococcus aureus Small Colony Variants (SCVs): a road map for the metabolic pathways involved in persistent infections

Staphylococcus aureus Small Colony Variants (SCVs): a road map for the metabolic pathways involved in persistent infections

Physiological, Biochemical and Phylogenetic Characterization of Extremely Halophilic Bacteria Isolated From Khewra Mine, Pakistan

Amino acids and proteomic acclimation of Staphylococcus aureus when incubated in a defined minimal medium supplemented with 5% sodium chloride

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