Archaeal lipids trace ecology and evolution of marine ammonia-oxidizing archaea

Significance

Archaeal lipids are ubiquitous in marine sediments and are commonly used to infer past marine sea surface temperatures. However, these molecules can also be used to investigate the ecological and evolutionary history of marine archaea. Here we utilized data science techniques to identify two distinct patterns of archaeal lipid distribution from globally distributed seawater and surface sediments, indicative of shallow and deep ecotypes in the modern oceans. Further investigation of ancient marine sediments across the Mesozoic–Cenozoic suggests that deep water AOAs were suppressed in global oceans during greenhouse climates, which has not been observed by traditional molecular evolutionary models. This perspective carries important implications for marine nitrogen and carbon cycling and the reconstruction of past ocean temperatures.

Abstract

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.