The Vertical Metabolic Activity and Community Structure of Prokaryotes along Different Water Depths in the Kermadec and Diamantina Trenches

Abstract

Prokaryotes play a key role in particulate organic matter's decomposition and remineralization processes in the vertical scale of seawater, and prokaryotes contribute to more than 70% of the estimated remineralization. However, little is known about the microbial community and metabolic activity of the vertical distribution in the trenches. The composition and distribution of prokaryotes in the water columns and benthic boundary layers of the Kermadec Trench and the Diamantina Trench were investigated using high-throughput sequencing and quantitative PCR, together with the Biolog Ecoplate^TM microplates culture to analyze the microbial metabolic activity. Microbial communities in both trenches were dominated by Nitrososphaera and Halobacteria in archaea, and by Alphaproteobacteria and Gammaproteobacteria in bacteria, and the microbial community structure was significantly different between the water column and the benthic boundary layer. At the surface water, amino acids and polymers were used preferentially; at the benthic boundary layers, amino acids and amines were used preferentially. Cooperative relationships among different microbial groups and their carbon utilization capabilities could help to make better use of various carbon sources along the water depths, reflected by the predominantly positive relationships based on the co-occurrence network analysis. In addition, the distinct microbial metabolic activity detected at 800 m, which was the lower boundary of the twilight zone, had the lowest salinity and might have had higher proportions of refractory carbon sources than the shallower water depths and benthic boundary layers. This study reflected the initial preference of the carbon source by the natural microbes in the vertical scale of different trenches and should be complemented with stable isotopic tracing experiments in future studies to enhance the understanding of the complex carbon utilization pathways along the vertical scale by prokaryotes among different trenches.

Keywords: Diamantina Trench; Kermadec Trench; benthic boundary layer; microbial metabolic activity; water column.

Figure 1

Map of the sampling stations used in this study.

Figure 2

The temperature, salinity, and inorganic nutrients of ambient water samples of the Kermadec Trench (A) and the Diamantina Trench (B). The black circle and triangle symbols stand for salinity and temperature, while the blank circle, triangle, and star symbols stand for NO₂⁻ + NO₃⁻, NH₄⁺, and PO₄³⁻, respectively.

Figure 3

Microbial community structure in the WC and BBL of the Kermadec Trench (A) and the Diamantina Trench (B). * and ** stand for p < 0.05 and p < 0.01. The Shannon index and Evenness index in the WC and BBL of the Kermadec Trench (C) and the Diamantina Trench (D). The black circle and square symbols stand for the Shannon index and Evenness index, respectively. Non-linear multidimensional scaling (nMDS) analysis of microbial communities in the WC and BBL of the Kermadec Trench (E) and the Diamantina Trench (F) based on Bray–Curtis distances.

Figure 4

The abundance of the 16S rRNA gene at the WC and BBL of the Kermadec Trench (A) and the Diamantina Trench (B). Biplot of the redundancy analysis integrating environmental parameters and the microbial communities in the WC and BBL of the Kermadec Trench (C) and the Diamantina Trench (D). * and ** stand for p < 0.05 and p < 0.01.

Figure 5

The networks analysis among archaeal and bacterial groups in the WC and BBL of the Kermadec Trench (A,B) and the Diamantina Trench (C,D). The network represents relationships between co-occurring ecosystems, the edges represent co-occurrence relationships consistent at the 0.6 correlation level, and the nodes represent archaeal and bacterial taxa.

Figure 6

Box plots of the microbial metabolic activity of AWCD (A,B), Richness index (C,D), Shannon index (E,F), and Simpson index (G,H) in the WC and BBL of the Kermadec Trench and the Diamantina Trench.

Figure 7

Box plots of the utilization capability of the six major carbon groups, carbohydrates (A,B), amino acids (C,D), polymers (E,F), carboxylic acids (G,H), phenolic acids (I,J), and amines (K,L) by microbes in the WC and the BBL of the Kermadec Trench (left panel) and Diamantina Trench (right panel).