Planktonic Archaeal Ether Lipid Origins in Surface Waters of the North Pacific Subtropical Gyre.

Fuyan Li,Edward F Delong,Andy Leu,Laura T Carlson,Anitra E Ingalls,Kirsten Poff

doi:10.3389/fmicb.2021.610675

Fuyan Li, Edward F Delong + Show 4 more

Open Access

https://doi.org/10.3389/fmicb.2021.610675

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Abstract

Thaumarchaeota and Thermoplasmatota are the most abundant planktonic archaea in the sea. Thaumarchaeota contain tetraether lipids as their major membrane lipids, but the lipid composition of uncultured planktonic Thermoplasmatota representatives remains unknown. To address this knowledge gap, we quantified archaeal cells and ether lipids in open ocean depth profiles (0–200 m) of the North Pacific Subtropical Gyre. Planktonic archaeal community structure and ether lipid composition in the water column partitioned into two separate clusters: one above the deep chlorophyll maximum, the other within and below it. In surface waters, Thermoplasmatota densities ranged from 2.11 × 106 to 6.02 × 106 cells/L, while Thaumarchaeota were undetectable. As previously reported for Thaumarchaeota, potential homologs of archaeal tetraether ring synthases were present in planktonic Thermoplasmatota metagenomes. Despite the absence of Thaumarchaeota in surface waters, measurable amounts of intact polar ether lipids were found there. Based on cell abundance estimates, these surface water archaeal ether lipids contributed only 1.21 × 10–9 ng lipid/Thermoplasmatota cell, about three orders of magnitude less than that reported for Thaumarchaeota cells. While these data indicate that even if some tetraether and diether lipids may be derived from Thermoplasmatota, they would only comprise a small fraction of Thermoplasmatota total biomass. Therefore, while both MGI Thaumarchaeota and MGII/III Thermoplasmatota are potential biological sources of archaeal GDGTs, the Thaumarchaeota appear to be the major contributors of archaeal tetraether lipids in planktonic marine habitats. These results extend and confirm previous reports of planktonic archaeal lipid sources, and further emphasize the need for Thermoplasmatota cultivation, to better characterize the membrane lipid constituents of marine planktonic Thermoplasmatota, and more precisely define the sources and patterns of archaeal tetraether lipid distributions in marine plankton.

Highlights

Marine planktonic Archaea are abundant in diverse marine planktonic environments (DeLong, 1992, 1998; Fuhrman et al, 1992; DeLong et al, 1994), and play important roles in the biogeochemical cycles of carbon and nitrogen (Ingalls et al, 2006; Falkowski et al, 2008; MartinCuadrado et al, 2008; Iverson et al, 2012)
The two other most abundant planktonic archaeal groups belong to the Thermoplasmatota, and include MGII Archaea (DeLong, 1992), which are more abundant in the surface and in the deep chlorophyll maximum (DCM) (Massana et al, 2000; DeLong et al, 2006; Mincer et al, 2007; Hugoni et al, 2013); and MGIII Archaea (Fuhrman and Davis, 1997), which can be detected throughout the water column but are found more frequently in deeper waters (Massana et al, 1997; DeLong et al, 2006; Haro-Moreno et al, 2017)
To further investigate the contribution of Marine Group I (MGI) Thaumarchaeota and MGII/III Thermoplasmatota to the production of ether lipids in the euphotic zone, we examined planktonic archaeal community profiles determined by amplicon sequence analyses, and the distribution of ether lipids (i.e., glycerol dialkyl glycerol tetraethers (GDGTs) and archeol) in high resolution depth profiles in the North Pacific Subtropical Gyre (NPSG) (Figure 1 and Supplementary Table 1)

Summary

Introduction

Marine planktonic Archaea are abundant in diverse marine planktonic environments (DeLong, 1992, 1998; Fuhrman et al, 1992; DeLong et al, 1994), and play important roles in the biogeochemical cycles of carbon and nitrogen (Ingalls et al, 2006; Falkowski et al, 2008; MartinCuadrado et al, 2008; Iverson et al, 2012). The most abundant group was originally called Marine Group I (MGI) planktonic Crenarchaeota (DeLong, 1992). This general phylogenetic group was later referred to as Thaumarchaeota as genomic analyses and protein phylogenies became available (Preston et al, 1996; Hallam et al, 2006a,b; Brochier-Armanet et al, 2008). The other GDGTs with cyclopentane rings are synthesized by other archaea including members of the Crenarchaeota and Euryarchaeota (Pearson and Ingalls, 2013)

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