skip to main content

Title: Archaeal lipids trace ecology and evolution of marine ammonia-oxidizing archaea
Archaeal membrane lipids are widely used for paleotemperature reconstructions, yet these molecular fossils also bear rich information about ecology and evolution of marine ammonia-oxidizing archaea (AOA). Here we identified thermal and nonthermal behaviors of archaeal glycerol dialkyl glycerol tetraethers (GDGTs) by comparing the GDGT-based temperature index (TEX 86 ) to the ratio of GDGTs with two and three cyclopentane rings (GDGT-2/GDGT-3). Thermal-dependent biosynthesis should increase TEX 86 and decrease GDGT-2/GDGT-3 when the ambient temperature increases. This presumed temperature-dependent (PTD) trend is observed in GDGTs derived from cultures of thermophilic and mesophilic AOA. The distribution of GDGTs in suspended particulate matter (SPM) and sediments collected from above the pycnocline—shallow water samples—also follows the PTD trend. These similar GDGT distributions between AOA cultures and shallow water environmental samples reflect shallow ecotypes of marine AOA. While there are currently no cultures of deep AOA clades, GDGTs derived from deep water SPM and marine sediment samples exhibit nonthermal behavior deviating from the PTD trend. The presence of deep AOA increases the GDGT-2/GDGT-3 ratio and distorts the temperature-controlled correlation between GDGT-2/GDGT-3 and TEX 86 . We then used Gaussian mixture models to statistically characterize these diagnostic patterns of modern AOA ecology from paleo-GDGT records to infer the evolution of marine AOA from the Mid-Mesozoic to the present. Long-term GDGT-2/GDGT-3 trends suggest a suppression of today’s deep water marine AOA during the Mesozoic–early Cenozoic greenhouse climates. Our analysis provides invaluable insights into the evolutionary timeline and the expansion of AOA niches associated with major oceanographic and climate changes.  more » « less
Award ID(s):
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Proceedings of the National Academy of Sciences
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The TEX86proxy, based on the distribution of isoprenoid glycerol dialkyl glycerol tetraethers (iGDGTs) from planktonic Thaumarchaeota, is widely used to reconstruct sea surface temperature (SST). Recent observations of species‐specific and regionally dependent TEX86‐SST relationships in cultures and the modern ocean raise the question of whether nonthermal factors may have impacted TEX86paleorecords. Here we evaluate the effects of ecological changes on TEX86using one Pliocene and two Pleistocene sapropels from the Mediterranean Sea. We find that TEX86‐derived SSTs deviate from‐derived SSTs before, during, and after each sapropel event.‐derived SSTs vary by less than 6 °C, while TEX86‐derived SSTs vary by up to 15 °C within a single record. Compound‐specific carbon isotope compositions indicate minimal confounding influence on TEX86from exogenous sources. Some of the variation can be accounted for by changes in nitrogen cycling intensity affecting thaumarchaeal iGDGT biosynthesis, as demonstrated by an inverse relationship between TEX86and δ15NTN. TEX86‐derived SSTs also consistently show warm anomalies in the Pleistocene, while the Pliocene samples exhibit both warmer and cooler relative offsets. These anomalies result from systematic differences between Plio‐Pleistocene iGDGT distributions and both modern Mediterranean and modern, globally distributed core top samples. Through characteristic GDGT distributions, we suggest the existence of three distinct endemic populations of Thaumarchaeota in the Pliocene, Pleistocene, and modern Mediterranean Sea, respectively. Importantly, these communities prevailed during both sapropel and oligotrophic conditions. Our results demonstrate that ecological and community‐specific effects must be considered when applying the TEX86proxy to paleorecords.

    more » « less

    Isoprenoid glycerol dialkyl glycerol tetraethers (iGDGTs) are commonly preserved molecular biomarkers of archaea whose distributions can be used to reconstruct past temperature, and possibly, methane and nitrogen cycling. To date, iGDGT systematics have not been widely investigated in Arctic lacustrine environments. Here, we analyze iGDGTs in sediments of Lake El'gygytgyn, located in the Russian Arctic, to reconstruct the paleoenvironmental conditions from the Pliocene to today using TEX86and other indices. The TEX86‐inferred temperature history shows a long‐term warming trend, in stark contrast to other Arctic records and other proxies from Lake El'gygytgyn, suggesting that non‐temperature factors obfuscate the use of TEX86at this site. Other GDGT‐based indices including the BIT Index, ΔRing Index, Methane Index and the GDGT‐0/crenarchaeol ratio suggest that TEX86is strongly influenced by archaeal community changes. The most significant community shifts are observedc. 2.4 Ma and record an increase in Euryarchaeota production and/or a decrease in Thaumarchaeota production, which was driven by the establishment of permafrost and perennial lake ice during the early Pleistocene. Overall, this study demonstrates an important interpretative framework for iGDGTs in lacustrine systems and describes variations in Arctic climate and lake biogeochemistry over timescales of thousands to millions of years.

    more » « less
  3. Glycerol dibiphytanyl glycerol tetraethers (GDGTs) are distinctive archaeal membrane-spanning lipids with up to eight cyclopentane rings and/or one cyclohexane ring. The number of rings added to the GDGT core structure can vary as a function of environmental conditions, such as changes in growth temperature. This physiological response enables cyclic GDGTs preserved in sediments to be employed as proxies for reconstructing past global and regional temperatures and to provide fundamental insights into ancient climate variability. Yet, confidence in GDGT-based paleotemperature proxies is hindered by uncertainty concerning the archaeal communities contributing to GDGT pools in modern environments and ambiguity in the environmental and physiological factors that affect GDGT cyclization in extant archaea. To properly constrain these uncertainties, a comprehensive understanding of GDGT biosynthesis is required. Here, we identify 2 GDGT ring synthases, GrsA and GrsB, essential for GDGT ring formation in Sulfolobus acidocaldarius . Both proteins are radical S-adenosylmethionine proteins, indicating that GDGT cyclization occurs through a free radical mechanism. In addition, we demonstrate that GrsA introduces rings specifically at the C-7 position of the core GDGT lipid, while GrsB cyclizes at the C-3 position, suggesting that cyclization patterns are differentially controlled by 2 separate enzymes and potentially influenced by distinct environmental factors. Finally, phylogenetic analyses of the Grs proteins reveal that marine Thaumarchaeota, and not Euryarchaeota, are the dominant source of cyclized GDGTs in open ocean settings, addressing a major source of uncertainty in GDGT-based paleotemperature proxy applications. 
    more » « less
  4. Summary

    Microorganisms regulate the composition of their membranes in response to environmental cues. Many Archaea maintain the fluidity and permeability of their membranes by adjusting the number of cyclic moieties within the cores of their glycerol dibiphytanyl glycerol tetraether (GDGT) lipids. Cyclized GDGTs increase membrane packing and stability, which has been shown to help cells survive shifts in temperature and pH. However, the extent of this cyclization also varies with growth phase and electron acceptor or donor limitation. These observations indicate a relationship between energy metabolism and membrane composition. Here we show that the average degree of GDGT cyclization increases with doubling time in continuous cultures of the thermoacidophileSulfolobus acidocaldarius(DSM 639). This is consistent with the behavior of a mesoneutrophile,Nitrosopumilus maritimusSCM1. Together, these results demonstrate that archaeal GDGT distributions can shift in response to electron donor flux and energy availability, independent of pH or temperature. Paleoenvironmental reconstructions based on GDGTs thus capture the energy available to microbes, which encompasses fluctuations in temperature and pH, as well as electron donor and acceptor availability. The ability of Archaea to adjust membrane composition and packing may be an important strategy that enables survival during episodes of energy stress.

    more » « less
  5. Abstract

    Many Archaea produce membrane‐spanning lipids that enable life in extreme environments. These isoprenoid glycerol dibiphytanyl glycerol tetraethers (GDGTs) may contain up to eight cyclopentyl and one cyclohexyl ring, where higher degrees of cyclization are associated with more acidic, hotter or energy‐limited conditions. Recently, the genes encoding GDGT ring synthases,grsAB, were identified in two Sulfolobaceae; however, the distribution and abundance ofgrshomologs across environments inhabited by these and related organisms remain a mystery. To address this, we examined the distribution ofgrshomologs in relation to environmental temperature and pH, from thermal springs across Earth, where sequences derive from metagenomes, metatranscriptomes, single‐cell and cultivar genomes. The abundance ofgrshomologs shows a strong negative correlation to pH, but a weak positive correlation to temperature. Archaeal genomes and metagenome‐assembled genomes (MAGs) that carry two or moregrscopies are more abundant in low pH springs. We also findgrsin 12 archaeal classes, with the most representatives in Thermoproteia, followed by MAGs of the uncultured Korarchaeia, Bathyarchaeia and Hadarchaeia, while several Nitrososphaeria encodes >3 copies. Our findings highlight the key role ofgrs‐catalysed lipid cyclization in archaeal diversification across hot and acidic environments.

    more » « less