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Metagenomics of Antarctic Marine Sediment Reveals Potential for Diverse Chemolithoautotrophy - PubMed

  • ️Fri Jan 01 2021

Metagenomics of Antarctic Marine Sediment Reveals Potential for Diverse Chemolithoautotrophy

Arkadiy I Garber et al. mSphere. 2021.

Abstract

The microbial biogeochemical processes occurring in marine sediment in Antarctica remain underexplored due to limited access. Further, these polar habitats are unique, as they are being exposed to significant changes in their climate. To explore how microbes drive biogeochemistry in these sediments, we performed a shotgun metagenomic survey of marine surficial sediment (0 to 3 cm of the seafloor) collected from 13 locations in western Antarctica and assembled 16 high-quality metagenome assembled genomes for focused interrogation of the lifestyles of some abundant lineages. We observe an abundance of genes from pathways for the utilization of reduced carbon, sulfur, and nitrogen sources. Although organotrophy is pervasive, nitrification and sulfide oxidation are the dominant lithotrophic pathways and likely fuel carbon fixation via the reverse tricarboxylic acid and Calvin cycles. Oxygen-dependent terminal oxidases are common, and genes for reduction of oxidized nitrogen are sporadically present in our samples. Our results suggest that the underlying benthic communities are well primed for the utilization of settling organic matter, which is consistent with findings from highly productive surface water. Despite the genetic potential for nitrate reduction, the net catabolic pathway in our samples remains aerobic respiration, likely coupled to the oxidation of sulfur and nitrogen imported from the highly productive Antarctic water column above. IMPORTANCE The impacts of climate change in polar regions, like Antarctica, have the potential to alter numerous ecosystems and biogeochemical cycles. Increasing temperature and freshwater runoff from melting ice can have profound impacts on the cycling of organic and inorganic nutrients between the pelagic and benthic ecosystems. Within the benthos, sediment microbial communities play a critical role in carbon mineralization and the cycles of essential nutrients like nitrogen and sulfur. Metagenomic data collected from sediment samples from the continental shelf of western Antarctica help to examine this unique system and document the metagenomic potential for lithotrophic metabolisms and the cycles of both nitrogen and sulfur, which support not only benthic microbes but also life in the pelagic zone.

Keywords: Antarctica; chemolithotrophy; marine microbiology; marine sediment; metagenomics.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIG 1
FIG 1

Map of Antarctica’s western peninsula, showing the geographic locations from which the metagenomic samples were derived.

FIG 2
FIG 2

Dot plots and redox cycling of various nitrogen (A) and sulfur (B) compounds. The various elemental species are colored blue and green (for nitrogen and sulfur, respectively) to visually separate them from the names of genes attributed to each reaction. Genes that appear to be abundant or consistently present through all or most of the sites are shown in bold in the redox cycling schematics above each dot plot. The size of each dot represents reads per million (RPM), a measure of gene abundance based on gene mapping, normalized to the length of each gene and size of the data set. The color gradients denote genes per million (GPM), a measure of gene diversity based on the number of different gene homologs identified, normalized to the total number of genes predicted from each metagenome.

FIG 3
FIG 3

Dot plots for the sugar transporters (A), carbon fixation (B), and hydrogenases (hyd.) (C) identified in the metagenome assemblies. As in Fig. 2, the size of each dot represents reads per million (RPM), a measure of gene abundance based on gene mapping, normalized to the length of each gene and size of the data set. The color gradients denote genes per million (GPM), a measure of gene diversity based on the number of different gene homologs identified, normalized to the total number of genes predicted from each metagenome.

FIG 4
FIG 4

Phylogenomic trees demonstrating the taxonomic context for (A) one high-quality archaeal MAG and (B) 15 high-quality bacterial MAGs reconstructed from WA.098.

FIG 5
FIG 5

Dot plots summarizing (A) energy sources and (B) terminal electron acceptors utilized by the 16 high-quality MAGs from WA.098. DMSO, dimethyl sulfoxide.

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