Archaeal Sources of Intact Membrane Lipid Biomarkers in the Oxygen Deficient Zone of the Eastern Tropical South Pacific.

Martina Sollai,Laura Villanueva,Jaap S Sinninghe Damsté,Ellen C Hopmans,Richard G Keil

doi:10.3389/fmicb.2019.00765

Abstract

Archaea are ubiquitous in the modern ocean where they are involved in the carbon and nitrogen biogeochemical cycles. However, the majority of Archaea remain uncultured. Archaeal specific membrane intact polar lipids (IPLs) are biomarkers of the presence and abundance of living cells. They comprise archaeol and glycerol dibiphytanyl glycerol tetraethers (GDGTs) attached to various polar headgroups. However, little is known of the IPLs of uncultured marine Archaea, complicating their use as biomarkers. Here, we analyzed suspended particulate matter (SPM) obtained in high depth resolution from a coastal and open ocean site in the eastern tropical South Pacific (ETSP) oxygen deficient zone (ODZ) with the aim of determining possible biological sources of archaeal IPL by comparing their composition by Ultra High Pressure Liquid Chromatography coupled to high resolution mass spectrometry with the archaeal diversity by 16S rRNA gene amplicon sequencing and their abundance by quantitative PCR. Thaumarchaeotal Marine Group I (MGI) closely related to Ca. Nitrosopelagicus and Nitrosopumilus dominated the oxic surface and upper ODZ water together with Marine Euryarchaeota Group II (MGII). High relative abundance of hexose phosphohexose- (HPH) crenarchaeol, the specific biomarker for living Thaumarchaeota, and HPH-GDGT-0, dihexose- (DH) GDGT-3 and -4 were detected in these water masses. Within the ODZ, DPANN (Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanoarchaeota, and Nanohaloarchaea) of the Woesearchaeota DHVE-6 group and Marine Euryarchaeota Group III (MGIII) were present together with a higher proportion of archaeol-based IPLs, which were likely made by MGIII, since DPANN archaea are supposedly unable to synthesize their own IPLs and possibly have a symbiotic or parasitic partnership with MGIII. Finally, in deep suboxic/oxic waters a different MGI population occurred with HPH-GDGT-1, -2 and DH-GDGT-0 and -crenarchaeol, indicating that here MGI synthesize membranes with IPLs in a different relative abundance which could be attributed to the different detected population or to an environmental adaptation. Our study sheds light on the complex archaeal community of one of the most prominent ODZs and on the IPL biomarkers they potentially synthesize.

Highlights

Archaea are numerous in the modern ocean (e.g., DeLong, 1992; Karner et al, 2001), where they constitute highly diverse communities and participate in the biogeochemical cycles of elements (Offre et al, 2013)
The biogeochemistry of the eastern tropical South Pacific (ETSP) oxygen deficient zone (ODZ) has been extensively studied with an emphasis on the nitrogen cycle
Thaumarchaeota have attracted most of the attention among archaea, because they perform the oxidation of ammonium to nitrite in a broad range of O2 regimes (Coolen et al, 2007; Lam et al, 2007, 2009; Beman et al, 2008; Molina et al, 2010; Pitcher et al, 2011b; Bristow et al, 2016)

Summary

Introduction

Archaea are numerous in the modern ocean (e.g., DeLong, 1992; Karner et al, 2001), where they constitute highly diverse communities (see Eme and Ford Doolittle, 2015 for a general review on the archaeal diversity) and participate in the biogeochemical cycles of elements (Offre et al, 2013). Marine Euryarchaeota Group II (MGII) and III (MGIII), whilst already detected by the pioneering studies of marine archaeal diversity (DeLong, 1992; Fuhrman et al, 1992), are yet to be isolated. The former group mostly includes motile photoheterotrophs living in the marine photic zone; other ecotypes, have been detected in deeper waters (Frigaard et al, 2006; Baker et al, 2013; Deschamps et al, 2014). Other uncultured planktonic archaeal lineages include members of the archaeal superphylum DPANN (Rinke et al, 2013; Castelle et al, 2015), which have recently been described as important components of the euxinic waters of the Black Sea (Sollai et al, 2018)

Methods

Results

Conclusion