Nitrogen and sulfur for phosphorus: Lipidome adaptation of anaerobic sulfate-reducing bacteria in phosphorus-deprived conditions

Author:

Ding Su1ORCID,Grossi Vincent2ORCID,Hopmans Ellen C.1ORCID,Bale Nicole J.1,Cravo-Laureau Cristiana3ORCID,Sinninghe Damsté Jaap S.14ORCID

Affiliation:

1. Department of Marine Microbiology and Biogeochemistry, NIOZ Royal Netherlands Institute for Sea Research, Texel SZ 1797, The Netherlands

2. Laboratoire de Géologie de Lyon: Terre, Planètes, Environnement, CNRS, Université Claude Bernard Lyon 1, Villeurbanne 69622, France

3. Institut des Sciences Analytiques et de Physico-chimie pour l’environnement et les Matériaux, Universite de Pau et des Pays de l’Adour, CNRS, Pau 64000, France

4. Department of Earth Sciences, Faculty of Geosciences, Utrecht University, Utrecht, CB 3584, The Netherlands

Abstract

Understanding how microbial lipidomes adapt to environmental and nutrient stress is crucial for comprehending microbial survival and functionality. Certain anaerobic bacteria can synthesize glycerolipids with ether/ester bonds, yet the complexities of their lipidome remodeling under varying physicochemical and nutritional conditions remain largely unexplored. In this study, we thoroughly examined the lipidome adaptations of Desulfatibacillum alkenivorans strain PF2803 T , a mesophilic anaerobic sulfate-reducing bacterium known for its high proportions of alkylglycerol ether lipids in its membrane, under various cultivation conditions including temperature, pH, salinity, and ammonium and phosphorous concentrations. Employing an extensive analytical and computational lipidomic methodology, we identified an assemblage of nearly 400 distinct lipids, including a range of glycerol ether/ester lipids with various polar head groups. Information theory-based analysis revealed that temperature fluctuations and phosphate scarcity profoundly influenced the lipidome’s composition, leading to an enhanced diversity and specificity of novel lipids. Notably, phosphorous limitation led to the biosynthesis of novel glucuronosylglycerols and sulfur-containing aminolipids, termed butyramide cysteine glycerols, featuring various ether/ester bonds. This suggests a novel adaptive strategy for anaerobic heterotrophs to thrive under phosphorus-depleted conditions, characterized by a diverse array of nitrogen- and sulfur-containing polar head groups, moving beyond a reliance on conventional nonphospholipid types.

Funder

EC | ERC | HORIZON EUROPE European Research Council

Publisher

Proceedings of the National Academy of Sciences

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