Mode of carbon and energy metabolism shifts lipid composition in the thermoacidophile Acidianus
Mode of carbon and energy metabolism shifts lipid composition in the thermoacidophile Acidianus
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DOI：
10.1128/aem.01369-23
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发表时间：
2024-01-18
影响因子：
4.4
通讯作者：
Leavitt，William D.
中科院分区：
文献类型：
--
作者：
Rhim，Jeemin H.;Zhou，Alice;Leavitt，William D.
环化的程度，或环指数（RI），在古细菌甘油二植烷甘油四醚（GDGT）脂质长期以来被认为是反映homeoviscussive适应温度。然而，最近的实验表明，其他因素（例如，pH、生长阶段和能量通量）也可以影响膜组成。本研究的主要目的是探讨碳和能量代谢对膜环化的影响。为此，我们培养了Acidianussp. DS 80是一种代谢灵活且嗜热嗜酸的古菌，其对不同的电子供体、受体和碳源组合（S 0/Fe 3 +/CO2、H2/Fe 3 +/CO2、H2/S 0/CO2或H2/S 0/葡萄糖）的作用。我们表明，在能量和碳代谢的差异，可能会导致超过一个完整的单位的RI的变化在thermoacidophileAcidianussp。DS80。RI的图案与电子供体和受体之间的归一化电子转移速率相关，并不总是与能量产率的热力学预测一致。有鉴于此，我们讨论了可能影响细胞能量代谢动力学的其他因素：电子转移链（ETC）效率、ETC反应组分的位置（细胞质与细胞外）以及电子供体和受体的物理状态（气体与固体）。此外，在异养过程中同化更多还原形式的碳似乎会减少脂质生物合成过程中对还原当量的需求，从而导致RI较低。总之，这些结果指出，在支配GDGT环化的细胞能量状态的基本作用，与那些经历更大的能量限制合成更多的环化GDGTs. IMPORTANCE一些古细菌独特的跨膜脂质不同数量的五元环或六元环的核心结构，调节膜的流动性和渗透性。膜核心脂质组成的变化反映了古细菌应对胁迫的基本适应策略，但多种环境和生理因素可能会影响膜流动性和渗透性的需求。在这项研究中，我们测试了如何Acidianussp.当与不同的电子供体/受体对生长时，DS 80改变了其核心脂质组成。我们发现，能量和碳代谢的变化显着影响的相对丰度环的核心脂质DS 80。这些观察结果强调，需要更好地约束代谢参数，除了环境因素，这可能会影响膜生理学的变化，在pedroea。这种考虑对于研究来自经历频繁环境波动和/或代谢多样性古菌茁壮成长的栖息地的古菌脂质特别重要。
The degree of cyclization, or ring index (RI), in archaeal glycerol dibiphytanyl glycerol tetraether (GDGT) lipids was long thought to reflect homeoviscous adaptation to temperature. However, more recent experiments show that other factors (e.g., pH, growth phase, and energy flux) can also affect membrane composition. The main objective of this study was to investigate the effect of carbon and energy metabolism on membrane cyclization. To do so, we cultivatedAcidianussp. DS80, a metabolically flexible and thermoacidophilic archaeon, on different electron donor, acceptor, and carbon source combinations (S0/Fe3+/CO2, H2/Fe3+/CO2, H2/S0/CO2, or H2/S0/glucose). We show that differences in energy and carbon metabolism can result in over a full unit of change in RI in the thermoacidophileAcidianussp. DS80. The patterns in RI correlated with the normalized electron transfer rate between the electron donor and acceptor and did not always align with thermodynamic predictions of energy yield. In light of this, we discuss other factors that may affect the kinetics of cellular energy metabolism: electron transfer chain (ETC) efficiency, location of ETC reaction components (cytoplasmicvs.extracellular), and the physical state of electron donors and acceptors (gasvs.solid). Furthermore, the assimilation of a more reduced form of carbon during heterotrophy appears to decrease the demand for reducing equivalents during lipid biosynthesis, resulting in lower RI. Together, these results point to the fundamental role of the cellular energy state in dictating GDGT cyclization, with those cells experiencing greater energy limitation synthesizing more cyclized GDGTs.IMPORTANCESome archaea make unique membrane-spanning lipids with different numbers of five- or six-membered rings in the core structure, which modulate membrane fluidity and permeability. Changes in membrane core lipid composition reflect the fundamental adaptation strategies of archaea in response to stress, but multiple environmental and physiological factors may affect the needs for membrane fluidity and permeability. In this study, we tested howAcidianussp. DS80 changed its core lipid composition when grown with different electron donor/acceptor pairs. We show that changes in energy and carbon metabolisms significantly affected the relative abundance of rings in the core lipids of DS80. These observations highlight the need to better constrain metabolic parameters, in addition to environmental factors, which may influence changes in membrane physiology in Archaea. Such consideration would be particularly important for studying archaeal lipids from habitats that experience frequent environmental fluctuations and/or where metabolically diverse archaea thrive.