Unique bacterial communities and lifestyles in deep ocean blue holes: Insights from the Yongle Blue Hole (South China Sea)

Abstract

Deep ocean blue holes possess steep physicochemical gradients, especially low dissolved oxygen concentration, which shape the extraordinary microbial communities. However, the environmental responses of microorganisms with different lifestyles and knowledge of culturable microorganisms in the blue holes are still unknown. Here, we investigated the bacterial community structure with different lifestyles of the world’s deepest blue hole - the Yongle Blue Hole (YBH) in the South China Sea using both culture-dependent and -independent methods. YBH can be divided by oxygen content into an oxic zone, a suboxic zone and two anoxic zones. The abundance of bacteria, archaea, genes dsrB and soxB were all higher in the free-living (FL) lifestyle than in the particle-associated (PA) lifestyle, yet the diversity and richness of PA bacteria were higher than that of FL bacteria. More Gammaproteobacteria and less Alphaproteobacteria, Chloroflexi and Nitrospinae were observed within the FL fraction than within the PA fraction. The relative abundance of sulfur-oxidizing bacteria (SOB) was dominant between 100-140 m (anoxic zone I) in YBH, with a maximum of 90.0% (140 m FL fraction). The SOB in YBH were mainly colorless sulfur bacteria and purple non-sulfur bacteria, of which Thiomicrorhabdus and Sulfurimonas were the main representatives. In addition, a total of 294 bacterial strains were isolated on a variety of media and culture conditions, and 22.2% (18/81) of anaerobic strains were identified as potential novel species. Our study reveals a distinction between FL and PA bacteria in YBH. It contributes to further understanding of the bacterial community in deep ocean blue holes, and provides bacterial resources for subsequent studies on their adaptation to extreme marine environments.

DNA metabarcoding reveals ecological patterns and driving mechanisms of archaeal, bacterial, and eukaryotic communities in sediments of the Sansha Yongle Blue Hole

“…Marine blue holes are generally characterized by steep physicochemical gradients within geographically restricted areas 1 , 13 , creating conditions for new, unidentified microbial lineages to exist 6 . High-quality metagenome-assembled genomes (MAGs) retrieved recently from the Amberjack Hole (Gulf of Mexico blue hole) showed that microbial communities were dominated by understudied microbial taxa, indicating high levels of novel microbial lineages in the Amberjack Hole 6 .…”

“…Numerous studies on water column microeukaryotic 9 , 10 and prokaryotic plankton 5 , 11 – 13 including bacteria and archaea have expanded our knowledge of the composition, structure, and potential function of the biological communities in the SYBH. The study by Liu et al 9 revealed obvious differences in the eukaryotic composition of the water column between the SYBH and the outer reef slope and demonstrated significant effects of turbidity and nitrite concentration on the eukaryotic community structure.…”

“…Nevertheless, limited information is available concerning the diversity, community structure and spatial distribution of eukaryotic communities in SYBH sediments, and what shapes the eukaryotic assemblages in the sediments remains unclear. For prokaryotes, studies on bacterial community revealed the vertical stratification of community composition in SYBH water column and highlighted the dominance of the phylum Proteobacteria 5 , 11 – 13 . Phylogenetic analysis indicated that the SYBH microbial ecosystem was characterized by the presence of unidentified microorganisms in the deep water layer 12 , and a considerable number of new taxa were identified among culturable anaerobic bacteria in SYBH water 13 .…”

“…For prokaryotes, studies on bacterial community revealed the vertical stratification of community composition in SYBH water column and highlighted the dominance of the phylum Proteobacteria 5 , 11 – 13 . Phylogenetic analysis indicated that the SYBH microbial ecosystem was characterized by the presence of unidentified microorganisms in the deep water layer 12 , and a considerable number of new taxa were identified among culturable anaerobic bacteria in SYBH water 13 . However, whether there are also abundant unknown prokaryotic taxa in SYBH sediments remains to be explored.…”

Seasonal and vertical variations of nutrient cycling in the world’s deepest blue hole

“…The existence of DO, even in trace amounts, has a significant influence on microbial composition and thus biogeochemical processes. For example, at the depth of 100-120 m in March 2017, the abundance of sulfur-oxidizing bacteria (SOB) was significantly higher than that of sulfate reduction bacteria (SRB) (Yao et al, 2020;Zhou et al, 2023). The SOB is a chemolithoautotrophic microorganism living in dysoxic or suboxic conditions and deriving energy from the oxidation of thiosulfate, sulfide, or elemental sulfur to sulfate (van Vliet et al, 2021).…”