Anoxia-adapted Cyanobacteria In A Marine Blue Hole

Vertical transmission of marine particles brings ocean surface cyanobacteria into the deep ocean, where heterotrophic cyanobacterial lineages probably evolve to adapt to new environments even in oxygen-depleted zones.

At present, active cyanobacteria have rarely been reported in dark and anoxic water columns in the deep sea. In this study, we recovered three metagenome-assembled genomes of cyanobacteria from the Yongle blue hole located in the South China Sea, two of which were actively transcribed in a dark, anoxic environment at 250 m depth, through integrated metagenomic and metatranscriptomic analyses of water samples from 21 stratified depths collected using in situ microbial fixation and filtration.

Relative abundance of Synechococcus MAGs in metagenomes and metatranscriptomes. (a) The division of oxic, suboxic, and anoxic zones in YBH. (b) The relative abundance of three Synechococcus MAGs across 21 metagenomes. (c) The relative abundance of three Synechococcus MAGs across 11 metatranscriptomes. Oxic-bin111 represents a Synechococcus genome reconstructed from the oxic layer, while Anoxic-bin48 and Anoxic-bin49 are two closely related Synechococcus genomes recovered from the anoxic layer. The samples marked with an asterisk (*) at the depth were collected in September, while the rest were collected in April 2021. — Applied and Environmental Microbiology

These anoxia-adapted cyanobacteria were phylogenetically approximate to the sponge cyanobacterial symbionts, while the genomic features showed similarities with both free-living and sponge symbiotic counterparts. They exhibit genomic features shared with symbiotic lineages, including loss of substrate utilization, biosynthesis pathways, DNA repair, and circadian regulation.

Conversely, they retain selected metabolic characteristics of free-living lineages, including phenylalanine biosynthesis and phosphoserine metabolism. Additionally, the discovery of taurine transport proteins in the genomes suggests the potential for organic sulfur uptake from the environment.

Altogether, these findings reveal a distinct genomic configuration in cyanobacteria inhabiting a permanently dark and anoxic marine system, characterized by the retention of oxygen-dependent metabolic potential alongside sustained transcriptional suppression under in situ conditions. This study provides new insights into the ecological persistence and evolutionary adaptation of cyanobacteria under long-term oxygen limitation.

Anoxia-adapted cyanobacteria in a marine blue hole, American Society for Microbiology

Astrobiology, genomics, extremophile,