Hydrothermally generated aromatic compounds are consumed by bacteria colonizing in Atlantis II Deep of the Red Sea

Abstract

Hydrothermal ecosystems have a wide distribution on Earth and many can be found in the basin of the Red Sea. Production of aromatic compounds occurs in a temperature window of ∼60-150 °C by utilizing organic debris. In the past 50 years, the temperature of the Atlantis II Deep brine pool in the Red Sea has increased from 56 to 68 °C, whereas the temperature at the nearby Discovery Deep brine pool has remained relatively stable at about 44 °C. In this report, we confirmed the presence of aromatic compounds in the Atlantis II brine pool as expected. The presence of the aromatic compounds might have disturbed the microbes in the Atlantis II. To show shifted microbial communities and their metabolisms, we sequenced the metagenomes of the microbes from both brine pools. Classification based on metareads and the 16S rRNA gene sequences from clones showed a strong divergence of dominant bacterial species between the pools. Bacteria capable of aromatic degradation were present in the Atlantis II brine pool. A comparison of the metabolic pathways showed that several aromatic degradation pathways were significantly enriched in the Atlantis II brine pool, suggesting the presence of aromatic compounds. Pathways utilizing metabolites derived from aromatic degradation were also significantly affected. In the Discovery brine pool, the most abundant genes from the microbes were related to sugar metabolism pathways and DNA synthesis and repair, suggesting a different strategy for the utilization of carbon and energy sources between the Discovery brine pool and the Atlantis II brine pool.

Figure 1

Aromatic compounds found in the ABP. The structures of the compounds were predicted on the basis of the data generated by the GC–MS analysis.

Figure 2

Bacterial genera in the Atlantis II Deep and Discovery Deep brine pools. Bacterial composition in the Atlantis II Deep (ABP) and Discovery (DBP) Deep brine pools was estimated by taxonomically classifying the 16S rRNA fragments identified from metadata reads. Classification at the genus level was performed by using the RDP classifier (Cole et al., 2009). No confidence threshold was applied to the classification, and the best match in the RDP database was used to determine the genus of a fragment. The percentages of bacterial 16S rRNA fragments are shown in parentheses. The minor groups refer to a collection of genera comprising <1% of the total 16S rRNA fragments in both samples. ^#Aromatic degrading bacterial genus; ^*heavy-metal-resistant bacterial genus.

Figure 3

Clustering of KEGG genes from the ABP and DBP in reference to three GOS data sets. Percentage of KEGG genes in the ABP and DBP metadata compared with those in the three reference GOS data sets. Only genes showing a >1% difference were used for the clustering. The color code indicates the relative abundance of the genes, ranging from green (low abundance) via black to red (high abundance).

Figure 4

KEGG maps showing significant differences in completeness between the ABP and DBP. Enriched KEGG genes (those with a copy number larger than the average number of all of the genes) were placed in KEGG maps with their EC numbers or KEGG annotations. Genes were ranked based on copy number. The top 10% of abundant genes were included in the pathway maps, and the node number of the maps recorded. Using a 10% increment of the top-ranking genes, 10 sets of node numbers for each KEGG map were obtained. The number of nodes in the Atlantis II (A) and Discovery (D) brine pools was compared using a Mann–Whitney U-test. The figure shows a map of the significant differences between the two samples (P<0.05). A KEGG map has many nodes, each of which represents a gene or cofactor. The increase in the number of nodes using a 20% gene increment is indicated by the color code. A white box indicates zero nodes. The names of KEGG pathways in the same functional categories are displayed in the same color.