Methylation at the C-2 position of hopanoids increases rigidity in native bacterial membranes

Wu, Chia-Hung; Bialecka-Fornal, Maja; Newman, Dianne K.

doi:10.7554/elife.05663

Cited by 40 publications

(52 citation statements)

References 54 publications

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“…Hopanoids have previously been demonstrated to help rigidify membranes (Sáenz, Sezgin, Schwille, & Simons, ; Wu, Bialecka‐Fornal, et al., ), so we hypothesized that their absence would affect the growth rate of N. punctiforme at extreme temperatures. To test this, we compared the doubling times of N. punctiforme S WT, shc, and hpnP at different temperatures.…”

Section: Resultsmentioning

confidence: 99%

“…Key to achieving a satisfying explanation is the need to understand hopanoid functions in diverse modern bacteria and to know which environmental conditions trigger their production. To date, studies using genetic and phenotypic analyses in Alphaproteobacteria have found that hopanoids are involved in membrane rigidity, stress tolerance, and symbiotic interactions (Kulkarni et al., ; Ricci et al., ; Sáenz et al., ; Schmerk et al., ; Silipo et al., ; Welander et al., ; Wu, Bialecka‐Fornal, et al., ). Although Alphaproteobacteria appear to be the dominant 2‐methylhopanoid producers in modern environments, as well as the group that first evolved the C‐2 methylase (Ricci, Michel, & Newman, ; Ricci et al., ), it has long been appreciated that cyanobacteria make 2‐methylhopanoids in significant abundance in some environments (Summons et al., ; Talbot et al., ).…”

Section: Discussionmentioning

confidence: 99%

“…A major constraint on our interpretative confidence arises from the fact that while hopanoids are made by phylogenetically diverse bacteria, to date, studies of hopanoid function have mainly been performed in Proteobacteria. Such work has shown that hopanoids assist in rigidifying cell membranes, aid in stress tolerance, and are important in facilitating plant–microbe symbioses (Kulkarni et al., , ; Ricci et al., ; Sáenz et al., ; Schmerk, Bernards, & Valvano, ; Silipo et al., ; Welander et al., ; Wu, Bialecka‐Fornal, & Newman, ). Although today Alphaproteobacteria appear to be the dominant producers of hopanoids in most environments (Pearson & Rusch, ; Ricci et al., ), cyanobacteria have long been known to contribute to hopanoid deposition in certain locales, such as Yellowstone National Park (Jahnke et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme

et al. 2016

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Hopanes are abundant in ancient sedimentary rocks at discrete intervals in Earth history, yet interpreting their significance in the geologic record is complicated by our incomplete knowledge of what their progenitors, hopanoids, do in modern cells. To date, few studies have addressed the breadth of diversity of physiological functions of these lipids and whether those functions are conserved across the hopanoid-producing bacterial phyla. Here, we generated mutants in the filamentous cyanobacterium, Nostoc punctiforme, that are unable to make all hopanoids (shc) or 2-methylhopanoids (hpnP). While the absence of hopanoids impedes growth of vegetative cells at high temperature, the shc mutant grows faster at low temperature. This finding is consistent with hopanoids acting as membrane rigidifiers, a function shared by other hopanoid-producing phyla. Apart from impacting fitness under temperature stress, hopanoids are dispensable for vegetative cells under other stress conditions. However, hopanoids are required for stress tolerance in akinetes, a resting survival cell type. While 2-methylated hopanoids do not appear to contribute to any stress phenotype, total hopanoids and to a lesser extent 2-methylhopanoids were found to promote the formation of cyanophycin granules in akinetes. Finally, although hopanoids support symbiotic interactions between Alphaproteobacteria and plants, they do not appear to facilitate symbiosis between N. punctiforme and the hornwort Anthoceros punctatus. Collectively, these findings support interpreting hopanes as general environmental stress biomarkers. If hopanoid-mediated enhancement of nitrogen-rich storage products turns out to be a conserved phenomenon in other organisms, a better understanding of this relationship may help us parse the enrichment of 2-methylhopanes in the rock record during episodes of disrupted nutrient cycling.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme

et al. 2016

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“…This observation decouples the evolution of ordered biochemically active liquid membranes from the requirement for molecular oxygen and suggests that the ability to subcompartmentalize membranes could have preceded the evolution of sterols. Subsequently, it was shown that hopanoidbased ordering can be tuned by structural modifications of their ring structure or polar side chain (16,17).…”

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confidence: 99%

Hopanoids as functional analogues of cholesterol in bacterial membranes

Sáenz

Grosser

Bradley

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

200

177

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The functionality of cellular membranes relies on the molecular order imparted by lipids. In eukaryotes, sterols such as cholesterol modulate membrane order, yet they are not typically found in prokaryotes. The structurally similar bacterial hopanoids exhibit similar ordering properties as sterols in vitro, but their exact physiological role in living bacteria is relatively uncharted. We present evidence that hopanoids interact with glycolipids in bacterial outer membranes to form a highly ordered bilayer in a manner analogous to the interaction of sterols with sphingolipids in eukaryotic plasma membranes. Furthermore, multidrug transport is impaired in a hopanoid-deficient mutant of the gram-negative Methylobacterium extorquens, which introduces a link between membrane order and an energy-dependent, membrane-associated function in prokaryotes. Thus, we reveal a convergence in the architecture of bacterial and eukaryotic membranes and implicate the biosynthetic pathways of hopanoids and other order-modulating lipids as potential targets to fight pathogenic multidrug resistance.

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“…Dried samples were stored at −20 °C and dissolved in 100 μL isopropanol/acetonitrile/water (2:1:1) for analysis by LC‐MS. Membranes were fractionated on a Percoll gradient as described (Wu et al ., ) to permit lipid analysis of the inner and outer membranes.…”

Section: Methodsmentioning

confidence: 99%

Lipid remodeling in Rhodopseudomonas palustris TIE‐1 upon loss of hopanoids and hopanoid methylation

et al. 2015

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The sedimentary record of molecular fossils (biomarkers) can potentially provide important insights into the composition of ancient organisms; however, it only captures a small portion of their original lipid content. To interpret what remains, it is important to consider the potential for functional overlap between different lipids in living cells, and how the presence of one type might impact the abundance of another. Hopanoids are a diverse class of steroid analogs made by bacteria and found in soils, sediments, and sedimentary rocks. Here, we examine the trade-off between hopanoid production and that of other membrane lipids. We compare lipidomes of the metabolically versatile α-proteobacterium Rhodopseudomonas palustris TIE-1 and two hopanoid mutants, detecting native hopanoids simultaneously with other types of polar lipids by electrospray ionization mass spectrometry. In all strains, the phospholipids contain high levels of unsaturated fatty acids (often >80%). The degree to which unsaturated fatty acids are modified to cyclopropyl fatty acids varies by phospholipid class. Deletion of the capacity for hopanoid production is accompanied by substantive changes to the lipidome, including a several-fold rise of cardiolipins. Deletion of the ability to make methylated hopanoids has a more subtle effect; however, under photoautotrophic growth conditions, tetrahymanols are upregulated twofold. Together, these results illustrate that the 'lipid fingerprint' produced by a micro-organism can vary depending on the growth condition or loss of single genes, reminding us that the absence of a biomarker does not necessarily imply the absence of a particular source organism.

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Methylation at the C-2 position of hopanoids increases rigidity in native bacterial membranes

Cited by 40 publications

References 54 publications

Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme

Hopanoids play a role in stress tolerance and nutrient storage in the cyanobacterium Nostoc punctiforme

Hopanoids as functional analogues of cholesterol in bacterial membranes

Lipid remodeling in Rhodopseudomonas palustris TIE‐1 upon loss of hopanoids and hopanoid methylation

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