Hopanoids Are Not Essential for Growth of Streptomyces scabies 87-22

Abstract

Hopanoids are triterpenoic, pentacyclic compounds that are structurally similar to sterols, which are required for normal cell function in eukaryotes. Hopanoids are thought to be an important component of bacterial cell membranes because they control membrane fluidity and diminish passive diffusion of ions, and a few taxons modulate their hopanoid content in response to environmental stimuli. However, to our knowledge, mutational studies to assess the importance of hopanoids in bacterial physiology have never been performed. Genome sequencing of the potato scab pathogen, Streptomyces scabies 87-22, revealed a hopanoid biosynthetic gene cluster (HBGC) that is predicted to synthesize hopene and aminotrihydroxybacteriohopane products. Hopene was produced by fully sporulated cultures of S. scabies on solid ISP4 (International Streptomyces Project 4) medium as well as by submerged mycelia grown in liquid minimal medium. The elongated hopanoid aminotrihydroxybacteriohopane was not detected under either growth condition. Transcription of the S. scabies HBGC was upregulated during aerial growth, which suggests a link between hopanoid production and morphological development. Functional analysis of the S. scabies ⌬hop615-1 and ⌬hop615-7 mutant strains, the first hopanoid mutants created in any bacterial taxon, revealed that hopanoids are not required for normal growth or for tolerance of ethanol, osmotic and oxidative stress, high temperature, or low pH. This suggests that hopanoids are not essential for normal streptomycete physiology.

Hopanoid Production Is Required for Low-pH Tolerance, Antimicrobial Resistance, and Motility in Burkholderia cenocepacia

“…One of the few studies utilizing a genetic approach to define the role of hopanoids in membrane structure-function reported that the loss of hopanoid production in Rhodopseudomonas palustris resulted in sensitivity to acidic and alkaline conditions, bile salts, and certain antibiotics (72). This increased sensitivity was not observed in similar experiments performed with Streptomyces scabies (62), demonstrating that hopanoid function varies depending on taxonomy, environment, and physiology.…”

“…From the sequenced genome of B. cenocepacia J2315, we identified several gene clusters encoding putative hopanoid biosynthesis and transport genes. To date, every bacterium whose genome contains hopanoid biosynthesis genes has been found to produce hopanoids (23,53,57,62,72). The key step in hopanoid biosynthesis is the conversion of linear squalene to the basic hopene structure, which is catalyzed by squalene-hopene cyclase (Fig.…”

Composite Bacterial Hopanoids and Their Microbial Producers across Oxygen Gradients in the Water Column of the California Current

“…Similar to the physiological role of sterols in eukaryotic membranes, BHPs appear to be involved primarily in membrane stabilization and were recently shown to have the same membrane-ordering properties as sterols (7). Unlike sterols in eukaryotic organisms, BHPs do not appear to be essential for overall cell growth and survival in bacteria (8,9), presumably because those that lack BHPs produce other membrane lipids to compensate. BHPs are also important in other membrane functions such as pH tolerance and antibiotic resistance (8,10), lipid raft formation (11), and late stationary-phase survival (12).…”

Exploring the distribution and physiological roles of bacterial membrane lipids in the marine environment

“…It has recently been shown that hopanoids are not essential for the growth of some hopanoid producing bacteria (Welander et al, 2009;Seipke and Loria, 2009), which suggests that the biological role of hopanoids is not essential for survival. But, it is also possible that although hopanoids may not be essential in euxinic cultures under conditions selected for optimal growth, that they might serve a function that is crucial for survival in the environment.…”