Abstract
Temperature exerts a first-order control on microbial populations, which constantly adjust the fluidity and permeability of their cell membrane lipids to minimize loss of energy by ion diffusion across the membrane. Analytical advances in liquid chromatography coupled to mass spectrometry have allowed the detection of a stunning diversity of bacterial and archaeal lipids in extreme environments such as hot springs, hydrothermal vents and deep subsurface marine sediments. Here, we investigated a thermal gradient from 18 to 101°C across a marine sediment field and tested the hypothesis that cell membrane lipids provide a major biochemical basis for the bioenergetics of archaea and bacteria under heat stress. This paper features a detailed lipidomics approach with the focus on membrane lipid structure-function. Membrane lipids analyzed here include polar lipids of bacteria and polar and core lipids of archaea. Reflecting the low permeability of their ether-linked isoprenoids, we found that archaeal polar lipids generally dominate over bacterial lipids in deep layers of the sediments influenced by hydrothermal fluids. A close examination of archaeal and bacterial lipids revealed a membrane quandary: not only low permeability, but also increased fluidity of membranes are required as a unified property of microbial membranes for energy conservation under heat stress. For instance, bacterial fatty acids were composed of longer chain lengths in concert with higher degree of unsaturation while archaea modified their tetraethers by incorporation of additional methyl groups at elevated sediment temperatures. It is possible that these configurations toward a more fluidized membrane at elevated temperatures are counterbalanced by the high abundance of archaeal glycolipids and bacterial sphingolipids, which could reduce membrane permeability through strong intermolecular hydrogen bonding. Our results provide a new angle for interpreting membrane lipid structure-function enabling archaea and bacteria to survive and grow in hydrothermal systems.
Highlights
Temperature exerts a first-order control on microbial populations, as cell physiology and biochemistry are adapted to specific temperature ranges (Rothschild and Mancinelli, 2001; Schrenk et al, 2008)
In addition to reporting the influence of source fluids, we suggest that temperature is one of the key factors controlling microbial populations in sediments of Spathi Bay, as it has been reported for other hydrothermal environments (Schrenk et al, 2008; Boyd et al, 2013; Cole et al, 2013; Sharp et al, 2014)
In order to cope with frequent changes in temperature, and in toxic conditions, bacteria and archaea inhabiting these sediments must continuously adapt their cell membrane lipid composition
Summary
Temperature exerts a first-order control on microbial populations, as cell physiology and biochemistry are adapted to specific temperature ranges (Rothschild and Mancinelli, 2001; Schrenk et al, 2008). The extraordinary proton conductance via the von Grotthuß mechanism can result in futile ion cycling, i.e., inadvertent passage of ions across the membrane (Konings et al, 1995; van de Vossenberg et al, 1995, 1999; Valentine, 2007; Valentine and Valentine, 2009; Yoshinaga et al, 2016) Environmental conditions, such as temperature and pH, are expected to dictate cell membrane lipid composition (e.g., fatty acid chain length, types of lipid headgroups), which in turn controls the maintenance and dissipation of ion gradients across biological membranes (i.e., cell bioenergetics)
Sign-in/Register to view highlights & summary Sign-in/Register to access full text options 
Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a call
