Lipid Biomarkers From Microbial Mats on the McMurdo Ice Shelf, Antarctica: Signatures for Life in the Cryosphere

Abstract

Persistent cold temperatures, a paucity of nutrients, freeze-thaw cycles, and the strongly seasonal light regime make Antarctica one of Earth's least hospitable surface environments for complex life. Cyanobacteria, however, are well-adapted to such conditions and are often the dominant primary producers in Antarctic inland water environments. In particular, the network of meltwater ponds on the 'dirty ice' of the McMurdo Ice Shelf is an ecosystem with extensive cyanobacteria-dominated microbial mat accumulations. This study investigated intact polar lipids (IPLs), heterocyte glycolipids (HGs), and bacteriohopanepolyols (BHPs) in combination with 16S and 18S rRNA gene diversity in microbial mats of twelve ponds in this unique polar ecosystem. To constrain the effects of nutrient availability, temperature and freeze-thaw cycles on the lipid membrane composition, lipids were compared to stromatolite-forming cyanobacterial mats from ice-covered lakes in the McMurdo Dry Valleys as well as from (sub)tropical regions and hot springs. The 16S rRNA gene compositions of the McMurdo Ice Shelf mats confirm the dominance of Cyanobacteria and Proteobacteria while the 18S rRNA gene composition indicates the presence of Ochrophyta, Chlorophyta, Ciliophora, and other microfauna. IPL analyses revealed a predominantly bacterial community in the meltwater ponds, with archaeal lipids being barely detectable. IPLs are dominated by glycolipids and phospholipids, followed by aminolipids. The high abundance of sugar-bound lipids accords with a predominance of cyanobacterial primary producers. The phosphate-limited samples from the (sub)tropical, hot spring, and Lake Vanda sites revealed a higher abundance of aminolipids compared to those of the nitrogen-limited meltwater ponds, affirming the direct affects that N and P availability have on IPL compositions. The high abundance of polyunsaturated IPLs in the Antarctic microbial mats suggests that these lipids provide an important mechanism to maintain membrane fluidity in cold environments. High abundances of HG keto-ols and HG keto-diols, produced by heterocytous cyanobacteria, further support these findings and reveal a unique distribution compared to those from warmer climates.

Keywords: Antarctica; bacteriohopanepolyol; cyanobacteria; heterocyte glycolipids; homeoviscous adaptation; intact polar lipid; microbial mats.

FIGURE 1

(A) The schematic figure of the sampling location on the McMurdo Ice Shelf (78.00’S, 165.30’E). Microbial mats were collected from meltwater ponds on the ‘dirty ice’ marked in red. The figure was modified from Hawes et al. (2018). (B) Schematic map of the investigated meltwater ponds in the ‘dirty ice’ (modified from Jackson et al., 2021).

FIGURE 2

The relative abundance (%) of bacterial 16S rRNA genes in microbial mat communities. Shown are the major bacterial phyla. Samples with sub-fix (N.) indicate ‘Nostoc spheres,’ which were collected in three different meltwater ponds. Detailed results from the 16S rRNA gene sequencing are provided in the supporting information. Note the broken axis between 1 and 39%.

FIGURE 3

Principal coordinates analysis (PCoA) of the 16S rRNA gene (A) and 18S rRNA gene community composition (B) and intact polar lipid analysis (C) from the microbial mats collected at the McMurdo Ice Shelf. Ellipses for Nostoc type samples (samples 2, 11, 13, and 14; red; see Table 1) and freshwater samples (blue; see Table 1) represent the 95% confidence interval and were calculated using build in function of the “vegan” package. Conductivity results are shown in Table 1. Results from New Pond and Skua Pond were excluded from the PCoA analysis due to missing environmental (New Pond) and rRNA gene sequence data (Skua Pond).

FIGURE 4

The relative abundance (%) of eukaryotic 18S rRNA genes in microbial mat communities. Shown are the major eukaryotic phyla. Detailed results from the 18S rRNA sequencing can be found in the supporting information. Samples with (N.) indicate ‘Nostoc spheres,’ which were collected in three different meltwater ponds.

FIGURE 5

Intact polar lipids head group distribution in the meltwater ponds from the McMurdo Ice Shelf (A). Samples with (N.) indicate ‘Nostoc spheres’, which were collected in three different meltwater ponds. Panel (B) shows the results from the three different Antarctic lakes: Lake Joyce (LJ), Lake Fryxell (LF), and Lake Vanda (LV). The brackets show the percentage of photosynthetically active radiation (PAR) that reached the microbial mats. The PAR was adopted from previous studies (Jungblut et al., 2016; Mackey et al., 2017b,2018; Matys et al., 2019). Panel (C) shows the relative abundance of IPLs in the microbial mats from the Yellowstone National Park (United States), Highborne Cay (Bahamas), and Hamelin Pool (Australia).

FIGURE 6

Heterocyte glycolipid distribution in the meltwater ponds from the McMurdo Ice Shelf (A). Samples with (N.) indicate ‘Nostoc spheres,’ which were collected in three different meltwater ponds. Panel (B) shows the results from the three different Antarctic lakes: Lake Joyce (LJ), Lake Fryxell (LF) and Lake Vanda (LV). The brackets show the percentage of photosynthetically active radiation (PAR) that reached the microbial mats. The PAR was adopted from previous studies (Jungblut et al., 2016; Mackey et al., 2017b,2018; Matys et al., 2019). HGs in LV 4.3% PAR were below detection limit. Panel (C) shows the relative abundance of HGs in the microbial mats from the Yellowstone National Park (United States), Highborne Cay (Bahamas), and Hamelin Pool (Australia). DE, deoxyhexose; P, pentose; Me-hexose, methyl-hexose.

FIGURE 7

Bacteriohopanepolyols composition in the microbial mats from the meltwater ponds (A). Samples with (N.) indicate ‘Nostoc spheres’ that were collected in three different meltwater ponds. Panel (B) shows the relative BHP distribution from the three different Antarctic lakes: Lake Joyce (LJ), Lake Fryxell (LF) and Lake Vanda (LV). The brackets show the percentage of photosynthetically active radiation (PAR) that reached the microbial mats. The PAR was adopted from previous studies (Jungblut et al., 2016; Mackey et al., 2017b,2018; Matys et al., 2019). Panel (C) shows the relative abundance of BHPs in the microbial mats from the Yellowstone National Park (United States), Highborne Cay (Bahamas), and Hamelin Pool (Australia).

FIGURE 8

Conceptual sketch of the presenting controlling environmental parameters and the corresponding lipid membrane signatures. Environmental parameters include light regime (hv⁺), temperature in cold (C; blue thermometer) and warm (H; red thermometer), ice coverage and nutrient (N-limiting or P-limiting) availability.