The diversity, community dynamics, and interactions of the microbiome in the world's deepest blue hole: insights into extreme environmental response patterns and tolerance of marine microorganisms

Abstract

This study comprehensively examined the community dynamics, functional profiles, and interactions of the microbiome in the world's deepest blue hole. The findings revealed a positive correlation between the α-diversities of Symbiodiniaceae and archaea, indicating the potential reliance of Symbiodiniaceae on archaea in an extreme environment resulting from a partial niche overlap. The negative association between the α-diversity and β-diversity of the bacterial community suggested that the change rule of the bacterial community was consistent with the Anna Karenina effects. The core microbiome comprised nine microbial taxa, highlighting their remarkable tolerance and adaptability to sharp environmental gradient variations. Bacteria and archaea played significant roles in carbon, nitrogen, and sulfur cycles, while fungi contributed to carbon metabolism. This study advanced our understanding of the community dynamics, response patterns, and resilience of microorganisms populating the world's deepest blue hole, thereby facilitating further ecological and evolutional exploration of microbiomes in diverse extreme environments.

Keywords: deepest blue hole; extreme environment; microbiome community dynamics; response pattern; tolerance threshold.

Fig 1

The location of the Sansha Yongle Blue Hole in the South China Sea. (a) The SYBH located in Xisha Islands, (b) which developed in reef platform of Yongle atoll. (c) The sampling depths of the SYBH. The map in panel a is republished from Frontiers in Microbiology (65).

Fig 2

The community composition of microbiome in Sansha Yongle Blue Hole. The taxonomic profile of the abundant communities of (a) Symbiodiniaceae, (b) bacteria, (c) archaea, and (d) fungi in distinct water layers (0–250 m) in the SYBH.

Fig 3

The microbiome community structure and relative dispersion in the Sansha Yongle Blue Hole. The non-metric multidimensional scaling (NMDS) of Bray-Curtis distances of the compositions of (a) Symbiodiniaceae-, (b) bacteria-, (c) archaea-, and (d) fungi-associated seawater samples in distinct depths in (YBH).

Fig 4

Environmental drivers of α-diversity and β-diversity for microbiome in the Sansha Yongle Blue Hole. Positive (orange) and negative (blue) Pearson’s correlation results comparing α-diversity and β-diversity of (a) Symbiodiniaceae, (c) bacteria, (e) archaea, and (g) fungi with distinct anaerobic (CH₄, sulfide, N₂O), physical [depth (m) temperature (Temp: °C), salinity (Sal: PSU), DO (mg/L), pH, Turb (FNU)], and nutrient [NO₃ ⁻ (μmol/L), NO₂ ⁻ (μmol/L), NH₄ ⁺(μmol/L), SiO₃ ²⁻ (μmol/L), PO₄ ³⁻ (μmol/L), DOC (μmol/L), POC (μmol/L), SPM (mg/L), Chl a (μg/L)] parameters at the SYBH. (b, d, f, h) The variation partitioning analysis of relative contribution of anaerobic, physical, and nutrient parameters in microbial β-diversity.

Fig 5

The community composition and change trend of core microbiome in the Sansha Yongle Blue Hole. (a–d) The pie chart on the top shows the percentage of core microbiome in microbial community composition. (e–m) The change trend of the relative abundance of core microbial ASV in SYBH.

Fig 6

Enrichment characteristics of functional traits in microbiome from the Sansha Yongle Blue Hole. Enrichment functional traits with LDA scores of 2 or greater in microbial communities of (a) bacteria, (b) archaea, and (c) fungi among different water layers. The functional profiling predicting of bacteria was used to PICRUST 2 and FAPROTAX, and those of archaea only was used to PICRUST 2. The function of fungi communities was predicted by FUNGuild.

Fig 7

The correlations of alpha diversity among microorganism in the Sansha Yongle Blue Hole. (a) Relationship of Shannon index (H′) between archaea and Symbiodiniaceae in the SYBH. (b) Correlation of Shannon index (H′) between fungi and bacteria in the SYBH.

Fig 8

The microbiota interaction network and complexity of microbial community in Sansha Yongle Blue Hole. (a) The microbial interaction network in different depths in SYBH. (b) The key microbial drivers of interaction network in the SYBH. (c) The changing rule of microbial network complexity in the SYBH.