Microbial membrane lipid adaptations to high hydrostatic pressure in the marine environment

Abstract

The deep-sea is characterized by extreme conditions, such as high hydrostatic pressure (HHP) and near-freezing temperature. Piezophiles, microorganisms adapted to high pressure, have developed key strategies to maintain the integrity of their lipid membrane at these conditions. The abundance of specific membrane lipids, such as those containing unsaturated and branched-chain fatty acids, rises with increasing HHP. Nevertheless, this strategy is not universal among piezophiles, highlighting the need to further understand the effects of HHP on microbial lipid membranes. Challenges in the study of lipid membrane adaptations by piezophiles also involve methodological developments, cross-adaptation studies, and insight into slow-growing piezophiles. Moreover, the effects of HHP on piezophiles are often difficult to disentangle from effects caused by low temperature that are often characteristic of the deep sea. Here, we review the knowledge of membrane lipid adaptation strategies of piezophiles, and put it into the perspective of marine systems, highlighting the future challenges of research studying the effects of HHP on the microbial lipid composition.

Biological functions at high pressure: transcriptome response of Shewanella oneidensis MR-1 to hydrostatic pressure relevant to Titan and other icy ocean worlds

“…To counter the loss of membrane fluidity, microorganisms respond by increasing the proportion of unsaturated, short chain, and branched chain fatty acids in their membranes (Tamby et al, 2022 ). Here, the fadL (LFC −1.04) gene, encoding a long-chain fatty acid transport protein was downregulated, while three other genes involved in fatty acids synthesis including fabF_2, acpS and fabH2 , increased in expression ( p < 0.05) but did not surpass the LFC threshold of 1 (LFC 0.75, 0.74, 0.83, respectively).…”

Changes in environmental and engineered conditions alter the plasma membrane lipidome of fractured shale bacteria

“…This drives adaptive morphological and physiological remodeling in the inhabitant microbiome. High temperature and low pressure exert a similar effect on the biophysical properties of the membrane, which is a disruption of acyl chain packing order, which results in an increase in fluidity ( 58 , 59 ). In response, bacteria primarily increase the proportion of saturated fatty acids in the bilayer.…”

“…In addition, temperature and pressure changes affect headgroup chemistry. In general, high temperature and pressure usually induce an overall increase in relative abundance of polar lipids in the membrane ( 59 , 61 ). Also, zwitterionic lipids, which possess balanced positive and negative charges, pack more densely than their anionic counterparts, hence are elevated in some bacteria under high temperature and low pressure ( 59 ).…”

Particulate Organic Matter in the Atacama Trench: Tracing Sources and Possible Transport Mechanisms to the Hadal Seafloor

“…For example, this could be driven by bacterial processes such as anammox leading to rapid nitrogen loss within a shallow layer of the sediment surface (Thamdrup et al., 2021). Other recent studies have also highlighted potential physiological adaptations of the benthic microbial community to the high‐pressure and low‐temperature present in the hadal realm though cell membrane lipid composition (Flores et al., 2022; Tamby et al., 2023), whereas long‐term selective forces, where co‐existing taxa are more dissimilar and the phylogenetic turnover is greater than expected over the redox zone, lead to large community shifts over time (Schauberger et al., 2023). Together, changes in the chemical composition of benthic microbes as well as their metabolisms could alter the overall elemental and stable isotope composition of sedimentary OM.…”