Benthic archaea as potential sources of tetraether membrane lipids in sediments across an oxygen minimum zone

Abstract

Abstract. Benthic archaea comprise a significant part of the total prokaryotic biomass in marine sediments. Recent genomic surveys suggest they are largely involved in anaerobic processing of organic matter, but the distribution and abundance of these archaeal groups are still largely unknown. Archaeal membrane lipids composed of isoprenoid diethers or tetraethers (glycerol dibiphytanyl glycerol tetraether, GDGT) are often used as archaeal biomarkers. Here, we compare the archaeal diversity and intact polar lipid (IPL) composition in both surface (0-0.5 cm) and subsurface (10-12 cm) sediments recovered within, just below, and well below the oxygen minimum zone (OMZ) of the Arabian Sea. Archaeal 16S rRNA gene amplicon sequencing revealed a predominance of Thaumarchaeota (Marine Group I, MG-I) in oxygenated sediments. Quantification of archaeal 16S rRNA and ammonia monoxygenase (amoA) of Thaumarchaeota genes and their transcripts indicated the presence of an active in situ benthic population, which coincided with a high relative abundance of hexose phosphohexose crenarchaeol, a specific biomarker for living Thaumarchaeota. On the other hand, anoxic surface sediments within the OMZ and all subsurface sediments were dominated by archaea belonging to the Miscellaneous Crenarchaeota Group (MCG), the Thermoplasmatales and archaea of the DPANN (superphylum grouping Micrarchaeota, Diapherotrites, Aenigmarchaeota, Nanohaloarchaeota, Parvarchaeota, Nanoarchaeota, Pacearchaeota and Woesearchaeota). Members of the MCG were diverse, with a dominance of subgroup MCG-12 in anoxic surface sediments. This coincided with a high relative abundance of IPL GDGT-0 with an unknown polar head group. Subsurface anoxic sediments were characterized by higher relative abundance of GDGT-0, -2 and -3 with dihexose IPL types, GDGT-0 with a cyclopentanetetraol molecule and hexose, as well as the presence of specific MCG subgroups, suggesting that these groups could be the biological sources of these archaeal lipids.

Biomarker evidence for the occurrence of anaerobic ammonium oxidation in the eastern Mediterranean Sea during Quaternary and Pliocene sapropel formation

“…This has been seen in the modern Cariaco Basin, where ladderanes are observed, but SC ladderanes are absent (Rush et al, 2012a). The presence of SC ladderanes at the onset and termination, yet absence in the core S5 record, could also corroborate the concept of "splitanoxia" (as proposed for S1 by Bianchi et al, 2006), which hypothesises for the first 100 to 1000+ years of sapropel formation euxinia was present as a mid-depth oxygen minimum zone rather than a continuation from the seafloor. During these periods where the water column was not fully euxinic, ladderanes would have been oxidised to SC ladderanes in the underlying waters, which would have contained a certain amount of available oxygen.…”

“…The flow rate was 0.2 mL min −1 . Positive ion electrospray ionisation settings were capillary temperature, 300 • C; sheath gas (N 2 ) pressure, 40 arbitrary units (AU); auxiliary gas (N 2 ) pressure, 10 AU; spray voltage, 4.5 kV; probe heater temperature, 50 • C; S-lens 70 V. Target lipids were analysed with a mass range of m/z 350-2000 (resolution 70 000 ppm at m/z 200), followed by data-dependent tandem MS 2 with parameters as described by Besseling et al (2018). The combined extracted ion currents (within 3 ppm) of the protonated, ammoniated, and sodiated adducts (m/z 547.472 + 564.499 + 569.454, respectively) were used to integrate BHT isomer.…”

A combined lipidomic and 16S rRNA gene amplicon sequencing approach reveals archaeal sources of intact polar lipids in the stratified Black Sea water column

“…To examine the distribution of archaeal IPLs across the Black Sea water column, 193 individual IPLs (Supporting Information Table S2) were targeted for analysis using UHPLC-HRMS (Besseling et al, 2018). Table 2 shows the distribution of the 38 individual archaeal IPLs that were actually detected.…”

“…These are reported as a heat map of the relative abundance (%) of the total amounts of each individual IPL over the full depth range. Most of the targeted archaeal IPLs have been detected previously in environmental IPL surveys (Besseling et al, 2018;Liu et al, 2012;Meador et al, 2015;Rossel, Elvert, Ramette, Boetius, & Hinrichs, 2011;Rossel et al, 2008;Schubotz, Wakeham, Lipp, Fredricks, & Hinrichs, 2009 GDGT-0 to GDGT-2 and crenarchaeol were detected with MH, DH, and HPH as headgroups; GDGT-3 and GDGT-4 only occurred TA B L E 1 Physical properties (potential density and oxygen concentration), absolute abundance of the archaeal 16S rRNA gene copies, and the distribution of the reads over the various detected archaeal phylogenetic groups per depth in the Black Sea water column at station PHOX2 with MH and DH headgroups. The detected IPL types included a number of different headgroups attached in various combinations to GDGT-0 to GDGT-4, crenarchaeol, OH-GDGT-0 to OH-GDGT-4, and archaeol as core apolar lipids (see Supporting Information Figure S1 for structures of core lipids).…”

“…Detected headgroups are as follows: monohexose (MH); dihexose (DH), here indicating two MH moieties when attached to crenarchaeol or the other GDGTs, or one DH moiety when attached to archaeol; hexose phosphohexose (HPH), corresponding to two headgroups, namely one MH group and one phosphatidyl MH; methyl-hexose phosphohexose (MeHPH); 2-phosphatidylglycerol (2PG); monohexose 2-phosphatidylglycerol (MH-2PG); hexose-glucuronic acid (HgluA); phospho-dihexose (PDH); phosphatidylglycerol (PG); phosphatidylethanolamine (PE); phosphatidylserine (PS). Most of the targeted archaeal IPLs have been detected previously in environmental IPL surveys (Besseling et al, 2018;Liu et al, 2012;Meador et al, 2015;Rossel, Elvert, Ramette, Boetius, & Hinrichs, 2011;Rossel et al, 2008;Schubotz, Wakeham, Lipp, Fredricks, & Hinrichs, 2009 GDGT-0 to GDGT-2 and crenarchaeol were detected with MH, DH, and HPH as headgroups; GDGT-3 and GDGT-4 only occurred TA B L E 1 Physical properties (potential density and oxygen concentration), absolute abundance of the archaeal 16S rRNA gene copies, and the distribution of the reads over the various detected archaeal phylogenetic groups per depth in the Black Sea water column at station PHOX2 with MH and DH headgroups. In addition, GDGT-0 to GDGT-2 also occurred as 2PG IPLs, and GDGT-1 and GDGT-2 as MH-2PG IPLs (Table 2).…”