The archaeal lipidome in estuarine sediment dominated by members of the Miscellaneous Crenarchaeotal Group

Abstract

The anoxic sediments of the White Oak River estuary comprise a distinctive sulfate-methane transition zone (SMTZ) and natural enrichment of the archaea affiliated with the Miscellaneous Crenarchaeotal Group (MCG). Archaeal biphytanes were generally depleted in (13) C, with δ(13) C values being less than -35‰, indicative of production by active sedimentary archaeal populations. Multivariate analysis of the downcore distributions of 63 lipid biomarkers identified three major groups of lipids that were enriched in the surface, SMTZ or subsurface depths. Intact polar lipids with phosphatidylglycerol headgroups and glycerol dibiphytanyl glycerol tetraethers containing one, two or three cyclopentane rings were enriched at the base of the SMTZ and likely represent the accumulated product of a small but active ANME-1 community. The recently identified butanetriol dibiphytanyl glycerol tetraethers (BDGT), which increased relatively to other lipids with depth, were correlated with the relative abundance of MCG in archaeal 16S rRNA clone libraries, and were (13) C depleted throughout the depth profile, suggesting BDGT lipids as putative biomarkers of an MCG community that may either be autotrophic or feeding on (13) C-depleted organic substrates transported by porewater.

Unusual Butane- and Pentanetriol-Based Tetraether Lipids in Methanomassiliicoccus luminyensis, a Representative of the Seventh Order of Methanogens

“…Such lipids were recently found in marine and estuarine sediments but have not previously been detected in cultured archaeal representatives (35)(36)(37). We further documented the distribution of butanetriol-based lipids in diverse marine sediments, which suggested the widespread presence of relatives of M. luminyensis.…”

“…In some samples, for instance in the equatorial Pacific, BDGTs were not detected, which is probably related to low total organic carbon (TOC) concentrations (29) and sulfate-reducing conditions (85) at this site. The relative abundance of BDGTs in the 12 samples analyzed in this study (Table 2) is much lower than that in the estuarine WOR sediments, where BDGTs accounted for 15% of the total archaeal core lipid pool on average (35). While these data indicate that the conditions in the WOR sediments select for the BDGT producers, the factors controlling the distribution of the seventh order of methanogens and how they compete with hydrogenotrophic and methylotrophic methanogens, as they require both H 2 and methanol, remain targets for future studies.…”

“…In fact, members of the "environmental clade" of Methanomassiliicoccales were previously assigned to TMEG (15). Although Methanomassiliicoccales were not specifically described in WOR sediments, which is likely due to the low coverage of commonly used primers for Methanomassiliicoccales, closely related clades such as MBG-D and TMEG were abundant in these samples (35,80). Indeed, we evaluated commonly used primers against Methanomassiliicoccales, including the one used to sequence archaea from WOR sediments (22,80), using TestPrime 1.0 and the SILVA SSU r126 RefNR database (81), and the coverage was only between 0.5% and 56% for zero mismatches.…”

“…Butane-and pentanetriol-based tetraether lipids have recently been identified in a number of environmental settings, such as deeply buried marine (36) and shallow estuarine (35) sediments. Meador et al (35) suggested a potential association of BDGTs with the miscellaneous crenarchaeotal group (MCG) due to the positive correlation of BDGT lipids with the relative abundance of MCG 16S rRNA sequences in microbial communities of estuarine sediments from the White Oak River, NC, USA (WOR). The authors further interpreted the notable 13 C depletion of BDGTs as evidence for BDGT producers being either autotrophs or heterotrophs feeding on 13 C-depleted substrates.…”

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

“…Archaeal diversity is currently determined through nucleic acid-based methods, but the characterization of other cellular biomarkers such as membrane lipids has proven to be also effective in tracking the presence of archaeal groups in different ecosystems (e.g., Coolen et al, 2004a;Ingalls et al, 2012;Meador et al, 2015;Pitcher et al, 2011;Sturt et al, 2004). One of the advantages of using lipid-based methods to determine the presence of archaeal groups is that lipids can be preserved in the sedimentary record.…”