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

Sáenz, James

doi:10.1575/1912/4081

Cited by 7 publications

(5 citation statements)

References 85 publications

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“…Lipids were extracted according to previously described methods (26). Total lipid extracts (TLEs) were redissolved in dichloromethane (DCM) to a concentration of 10 mg/ml and stored at Ϫ20°C until further analysis.…”

Section: Methodsmentioning

confidence: 99%

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

Kharbush

Ugalde

Hogle

et al. 2013

Appl Environ Microbiol

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bHopanoids are pentacyclic triterpenoid lipids produced by many prokaryotes as cell membrane components. The structural variations of composite hopanoids, or bacteriohopanepolyols (BHPs), produced by various bacterial genera make them potentially useful molecular biomarkers of bacterial communities and metabolic processes in both modern and ancient environments. Building on previous work suggesting that organisms in low-oxygen environments are important contributors to BHP production in the marine water column and that there may be physiological roles for BHPs specific to these environments, this study investigated the relationship between trends in BHP structural diversity and abundance and the genetic diversity of BHP producers for the first time in a low-oxygen environment of the Eastern Tropical North Pacific. Amplification of the hopanoid biosynthesis gene for squalene hopene cyclase (sqhC) indicated far greater genetic diversity than would be predicted by examining BHP structural diversity alone and that greater sqhC genetic diversity exists in the marine environment than is represented by cultured representatives and most marine metagenomes. In addition, the genetic relationships in this data set suggest microaerophilic environments as potential "hot spots" of BHP production. Finally, structural analysis of BHPs showed that an isomer of the commonly observed BHP bacteriohopanetetrol may be linked to a producer that is more abundant in low-oxygen environments. Results of this study increase the known diversity of BHP producers and provide a detailed phylogeny with implications for the role of hopanoids in modern bacteria, as well as the evolutionary history of hopanoid biosynthesis, both of which are important considerations for future interpretations of the marine sedimentary record.

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Section: Methodsmentioning

confidence: 99%

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

Kharbush

Ugalde

Hogle

et al. 2013

Appl Environ Microbiol

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“…Biomass was harvested by filtration through two stacked, combusted glass fiber filters (GF‐75, 0.3 µm pore size; Advantec MFS). Lipids were extracted using a four‐step Bligh and Dyer extraction (Bligh & Dyer, 1959) using an ultrasonic bath and as modified by Sturt et al (2004) and Sáenz (2010). The total lipid extracts (TLEs) were gently dried under N 2 , reconstituted in dichloromethane:methanol 5:1, and stored at −20°C.…”

Section: Methodsmentioning

confidence: 99%

Marine and terrestrial nitrifying bacteria are sources of diverse bacteriohopanepolyols

et al. 2022

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Hopanoid lipids, bacteriohopanols and bacteriohopanepolyols, are membrane components exclusive to bacteria. Together with their diagenetic derivatives, they are commonly used as biomarkers for specific bacterial groups or biogeochemical processes in the geologic record. However, the sources of hopanoids to marine and freshwater environments remain inadequately constrained. Recent marker gene studies suggest a widespread potential for hopanoid biosynthesis in marine bacterioplankton, including nitrifying (i.e., ammonia‐ and nitrite‐oxidizing) bacteria. To explore their hopanoid biosynthetic capacities, we studied the distribution of hopanoid biosynthetic genes in the genomes of cultivated and uncultivated ammonia‐oxidizing (AOB), nitrite‐oxidizing (NOB), and complete ammonia‐oxidizing (comammox) bacteria, finding that biosynthesis of diverse hopanoids is common among seven of the nine presently cultivated clades of nitrifying bacteria. Hopanoid biosynthesis genes are also conserved among the diverse lineages of bacterial nitrifiers detected in environmental metagenomes. We selected seven representative NOB isolated from marine, freshwater, and engineered environments for phenotypic characterization. All tested NOB produced diverse types of hopanoids, with some NOB producing primarily diploptene and others producing primarily bacteriohopanepolyols. Relative and absolute abundances of hopanoids were distinct among the cultures and dependent on growth conditions, such as oxygen and nitrite limitation. Several novel nitrogen‐containing bacteriohopanepolyols were tentatively identified, of which the so called BHP‐743.6 was present in all NOB. Distinct carbon isotopic signatures of biomass, hopanoids, and fatty acids in four tested NOB suggest operation of the reverse tricarboxylic acid cycle in Nitrospira spp. and Nitrospina gracilis and of the Calvin–Benson–Bassham cycle for carbon fixation in Nitrobacter vulgaris and Nitrococcus mobilis. We suggest that the contribution of hopanoids by NOB to environmental samples could be estimated by their carbon isotopic compositions. The ubiquity of nitrifying bacteria in the ocean today and the antiquity of this metabolic process suggest the potential for significant contributions to the geologic record of hopanoids.

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“…Biomass was collected using filtration. Lipids were extracted using a Bligh and Dyer extraction (104) following the modifications of Sturt et al (105) and Saénz (106). Stable carbon isotopic composition of dissolved inorganic carbon, lipids, and biomass was analyzed using mass spectrometry.…”

Section: Methodsmentioning

confidence: 99%

Vitamin B ₁₂ -dependent biosynthesis ties amplified 2-methylhopanoid production during oceanic anoxic events to nitrification

Elling

Hemingway

Evans

et al. 2020

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

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Bacterial hopanoid lipids are ubiquitous in the geologic record and serve as biomarkers for reconstructing Earth’s climatic and biogeochemical evolution. Specifically, the abundance of 2-methylhopanoids deposited during Mesozoic ocean anoxic events (OAEs) and other intervals has been interpreted to reflect proliferation of nitrogen-fixing marine cyanobacteria. However, there currently is no conclusive evidence for 2-methylhopanoid production by extant marine cyanobacteria. As an alternative explanation, here we report 2-methylhopanoid production by bacteria of the genus Nitrobacter, cosmopolitan nitrite oxidizers that inhabit nutrient-rich freshwater, brackish, and marine environments. The model organism Nitrobacter vulgaris produced only trace amounts of 2-methylhopanoids when grown in minimal medium or with added methionine, the presumed biosynthetic methyl donor. Supplementation of cultures with cobalamin (vitamin B12) increased nitrite oxidation rates and stimulated a 33-fold increase of 2-methylhopanoid abundance, indicating that the biosynthetic reaction mechanism is cobalamin dependent. Because Nitrobacter spp. cannot synthesize cobalamin, we postulate that they acquire it from organisms inhabiting a shared ecological niche—for example, ammonia-oxidizing archaea. We propose that during nutrient-rich conditions, cobalamin-based mutualism intensifies upper water column nitrification, thus promoting 2-methylhopanoid deposition. In contrast, anoxia underlying oligotrophic surface ocean conditions in restricted basins would prompt shoaling of anaerobic ammonium oxidation, leading to low observed 2-methylhopanoid abundances. The first scenario is consistent with hypotheses of enhanced nutrient loading during OAEs, while the second is consistent with the sedimentary record of Pliocene–Pleistocene Mediterranean sapropel events. We thus hypothesize that nitrogen cycling in the Pliocene–Pleistocene Mediterranean resembled modern, highly stratified basins, whereas no modern analog exists for OAEs.

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

Cited by 7 publications

References 85 publications

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

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

Marine and terrestrial nitrifying bacteria are sources of diverse bacteriohopanepolyols

Vitamin B ₁₂ -dependent biosynthesis ties amplified 2-methylhopanoid production during oceanic anoxic events to nitrification

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

Cited by 7 publications

References 85 publications

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

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

Marine and terrestrial nitrifying bacteria are sources of diverse bacteriohopanepolyols

Vitamin B 12 -dependent biosynthesis ties amplified 2-methylhopanoid production during oceanic anoxic events to nitrification

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Vitamin B ₁₂ -dependent biosynthesis ties amplified 2-methylhopanoid production during oceanic anoxic events to nitrification