Intact polar lipids of Thaumarchaeota and anammox bacteria as indicators of N cycling in the eastern tropical North Pacific oxygen-deficient zone

Abstract

Abstract. In the last decade our understanding of the marine nitrogen cycle has improved considerably thanks to the discovery of two novel groups of microorganisms: ammoniaoxidizing archaea (AOA) and anaerobic ammonia-oxidizing (anammox) bacteria. Both groups are important in oxygendeficient zones (ODZs), where they substantially affect the marine N budget. These two groups of microbes are also well known for producing specific membrane lipids, which can be used as biomarkers to trace their presence in the environment. We investigated the occurrence and distribution of AOA and anammox bacteria in the water column of the eastern tropical North Pacific (ETNP) ODZ, one of the most prominent ODZs worldwide. Suspended particulate matter (SPM) was collected at different depths of the water column in high resolution, at both a coastal and an open-ocean setting. The SPM was analyzed for AOA-and anammox bacteria-specific intact polar lipids (IPLs), i.e., hexose-phosphohexose (HPH)-crenarchaeol and phosphatidylcholine (PC)-monoether ladderane. Comparison with oxygen profiles reveals that both the microbial groups are able to thrive at low ( < 1 µM) concentrations of oxygen. Our results indicate a clear niche segregation of AOA and anammox bacteria in the coastal waters of the ETNP but a partial overlap of the two niches of these microbial species in the open-water setting. The latter distribution suggests the potential for an interaction between the two microbial groups at the open-ocean site, although the nature of this hypothetical interaction (i.e., either competition or cooperation) remains unclear.

Intact polar lipids in the water column of the eastern tropical North Pacific: abundance and structural variety of non-phosphorus lipids

“…IP-GDGTs with the hexosephosphate-hexose (HPH) head groups and the core GDGT crenarchaeol (Fig. S4) of thaumarchaeota (Schouten et al, 2008;Elling et al, 2017) were most abundant at depths of nitrate maxima at all ETNP stations, as they are in other oxygen-deficient water columns (e.g., Pitcher et al, 2011;Lengger et al, 2012;Schouten et al, 2012;Sollai et al, 2015), although they were present at greater depths in the ENTP as well. The microbial enumerations by had shown previously that thaumarchaeota (referred to as crenarchaeota) and Euryarchaeota constitute almost equal amounts to <10 % of total cell number in the upper OMZ of the ETNP.…”

“…Important prokaryote-mediated processes within OMZs include denitrification and the anaerobic oxidation of ammonium (anammox), which together may account for 30 %-50 % of the total nitrogen loss from the ocean to the atmosphere (Gruber, 2008;Lam and Kuypers, 2011). Modern day OMZs comprise ∼ 8 % of global ocean volume (Karstensen et al, 2008;Paulmier and Ruiz-Pino, 2009;Lam and Kuypers, 2011), but any expansion in the coming decades as a consequence of global warming and increased stratification (Stramma et al, 2008;Keeling et al, 2010) would have profound effects on marine ecology, oceanic productivity, global carbon and nitrogen cycles, the biological pump and sequestration of carbon (Karstensen et al, 2008;Stramma et al, 2010;Wright et al, 2012). A better understanding of the effect of low O 2 on marine biogeochemistry and microbial ecology is thus warranted.…”

“…IPLs represent a diverse range of molecular structures, including phosphatidyl, glycosidic, phospho-glycosidic, and amino acid polar head groups linked to glyceryl-acyl and glyceryl-O-alkyl apolar moieties. IPL distributions have been documented in surface waters of the eastern subtropical South Pacific (Van Mooy and Fredricks, 2010), the western North Atlantic Ocean (Van Mooy et al, 2006Popendorf et al, 2011a), the South Pacific Ocean (Kharbush et al, 2016), the Mediterranean Sea (Popendorf et al, 2011b), the North Sea (Brandsma et al, 2012), lakes (Bale et al, 2016, the western English Channel (White et al, 2015) and throughout the water columns of stratified water bodies (Ertefai et al, 2008;Schubotz et al, 2009;Wakeham et al, 2012;Pitcher et al, 2011;Xie et al, 2014;Basse et al, 2014;Sollai et al, 2015). Surface waters are typically dominated by nine IPL classes.…”

“…Betaine lipids are widely distributed in lower plants and green algae (Dembitsky, 1996) and are thus usually assigned to eukaryotic algae in the ocean (Popendorf et al, 2011a), but DGTS was recently also found in bacteria where phosphorus is limited (Yao et al, 2015;Sebastian et al, 2016). Three commonly detected phospholipids are diacylglycerol phosphatidyl choline (PC-DAG, often simply referred to elsewhere as PC), phosphatidyl ethanolamine (PE-DAG, often PE), and phosphatidyl glycerol (PG-DAG, often PG), all of which have mixed eukaryotic or bacterial sources in the upper water column (Sohlenkamp et al, 2003;Popendorf et al, 2011a). Microbial source assignments have been broadly confirmed by isotope labeling studies (Popendorf et al, 2011a).…”

“…IPLs that are unique to marine archaea are comprised of glycerol dialkyl glycerol tetraether (GDGT) core lipids with various glycosidic, diglycosidic and mixed phospho-glyco polar head groups (e.g., Schouten et al, 2008;Pitcher et al, 2011;Zhu et al, 2016;Elling et al, 2017). Abundances of archaeal IP-GDGTs vary considerably with depth but are typically elevated in zones of water column oxygen depletion, especially where ammonium-oxidizing thaumarchaeota are abundant (Pitcher et al, 2011;Schouten et al, 2012;Sollai et al, 2015).…”