Proliferation of hydrocarbon-degrading microbes at the bottom of the Mariana Trench

Abstract

Background: The Mariana Trench is the deepest known site in the Earth's oceans, reaching a depth of ~ 11,000 m at the Challenger Deep. Recent studies reveal that hadal waters harbor distinctive microbial planktonic communities. However, the genetic potential of microbial communities within the hadal zone is poorly understood.

Results: Here, implementing both culture-dependent and culture-independent methods, we perform extensive analysis of microbial populations and their genetic potential at different depths in the Mariana Trench. Unexpectedly, we observed an abrupt increase in the abundance of hydrocarbon-degrading bacteria at depths > 10,400 m in the Challenger Deep. Indeed, the proportion of hydrocarbon-degrading bacteria at > 10,400 m is the highest observed in any natural environment on Earth. These bacteria were mainly Oleibacter, Thalassolituus, and Alcanivorax genera, all of which include species known to consume aliphatic hydrocarbons. This community shift towards hydrocarbon degraders was accompanied by increased abundance and transcription of genes involved in alkane degradation. Correspondingly, three Alcanivorax species that were isolated from 10,400 m water supplemented with hexadecane were able to efficiently degrade n-alkanes under conditions simulating the deep sea, as did a reference Oleibacter strain cultured at atmospheric pressure. Abundant n-alkanes were observed in sinking particles at 2000, 4000, and 6000 m (averaged 23.5 μg/gdw) and hadal surface sediments at depths of 10,908, 10,909, and 10,911 m (averaged 2.3 μg/gdw). The δ²H values of n-C_16/18 alkanes that dominated surface sediments at near 11,000-m depths ranged from - 79 to - 93‰, suggesting that these sedimentary alkanes may have been derived from an unknown heterotrophic source.

Conclusions: These results reveal that hydrocarbon-degrading microorganisms are present in great abundance in the deepest seawater on Earth and shed a new light on potential biological processes in this extreme environment.

Keywords: Challenger Deep; Hadal water; Hydrocarbon biosynthesis; Hydrocarbon degradation; Mariana Trench; Metagenomics; Microbial community.

Fig. 1

The composition of dominant microbial groups (top 30 abundant across all samples). a Microbial community shifts at order level with depth. b Microbial community shifts at genus level with depth. The analysis is based on the metagenomic data annotation against the NCBI-nr database. Sample names are defined by size fraction and sampling depth, e.g., FL10500 is the free-living fraction at 10,500 m. Dot size in the panel a is proportional to the relative abundance of microbial groups. The relative abundance at the genus level was rank transformed. The genera shadowed in blue indicate significant enrichment in the four NBW samples. The bar plot at the right side shows the average proportion (across the four NBW samples) of each genus in the total microbial population

Fig. 2

The relative abundance of three major COG categories related to amino acid transport and metabolism (E), carbohydrate transport and metabolism (G), and cell motility (N). FL, free living; PA, particle associated

Fig. 3

Hydrocarbon degradation pathways are present in the five high-quality metagenome assembled genomes (MAGs) belonging to Oceanospirillales. Predicted metabolic pathways and corresponding proteins in a given bacterial genome are indicated by colored dots to demonstrate the comparison between MAGs. The predictions are based on RAST and KEGG annotation. All five MAGs contained potential complete set of enzymes required for alkane degradation

Fig. 4

The relative abundance and expression of genes associated with aliphatic hydrocarbon degradation increase in NBW. a The relative abundance of genes at different depths. b The top five affiliated genera of each gene are shown in the heat map. c Transcript abundance of alkB and almA in free-living samples from different depths. Asterisks in panel a indicate statistically significant difference in gene abundance between the two zones

Fig. 5

Alkanes are degraded by Oceanospirillales isolates. a Bacterial degradation rate of C_18–38 n-alkanes at 4 °C, 0.1 MPa for 30 days. b n-eicosane at 4 °C, 60 MPa for 20 days for Alcanivorax strains (ZYF844, ZYF848, ZYF854), and 16 °C, 0.1 MPa for 12 days for O. marinus DSM 24913

Fig. 6

Alkanes accumulate at lower depths. a Sinking particle samples. b Surface sediment samples. Total n-alkane concentrations of each sample are shown in the upper-right corner of a and b

Fig. 7

The carbon and hydrogen isotopic compositions of n-C₁₆ and n-C₁₈ alkanes from hadal surface sediments. The errors are based on duplicate measurements