Distribution and Niche Separation of Planktonic Microbial Communities in the Water Columns from the Surface to the Hadal Waters of the Japan Trench under the Eutrophic Ocean

Abstract

The Japan Trench is located under the eutrophic Northwestern Pacific while the Mariana Trench that harbors the unique hadal planktonic biosphere is located under the oligotrophic Pacific. Water samples from the sea surface to just above the seafloor at a total of 11 stations including a trench axis station, were investigated several months after the Tohoku Earthquake in March 2011. High turbidity zones in deep waters were observed at most of the sampling stations. The small subunit (SSU) rRNA gene community structures in the hadal waters (water depths below 6000 m) at the trench axis station were distinct from those in the overlying meso-, bathy and abyssopelagic waters (water depths between 200 and 1000 m, 1000 and 4000 m, and 4000 and 6000 m, respectively), although the SSU rRNA gene sequences suggested that potential heterotrophic bacteria dominated in all of the waters. Potential niche separation of nitrifiers, including ammonia-oxidizing archaea (AOA), was revealed by quantitative PCR analyses. It seems likely that Nitrosopumilus-like AOAs respond to a high flux of electron donors and dominate in several zones of water columns including shallow and very deep waters. This study highlights the effects of suspended organic matter, as induced by seafloor deformation, on microbial communities in deep waters and confirm the occurrence of the distinctive hadal biosphere in global trench environments hypothesized in the previous study.

Keywords: deep ocean; hadal; niche separation; nitrification; trench.

FIGURE 1

Microbial cell and viral abundance and virus-prokaryote ratio throughout the water columns in the Japan Trench region. Each color indicates the sampling stations and the sampling time (days) after the Tohoku Earthquake on March 11, 2011.

FIGURE 2

Relative abundance of the archaeal SSU rRNA gene in the whole prokaryotic SSU rRNA gene assemblage, as estimated by quantitative PCR of the SSU rRNA gene throughout the water column in the Japan Trench region. The sampling time (days) after the Tohoku Earthquake on 11 March, 2011, is shown in the parentheses. Water samples from the deepest depth for each station were taken above 10 m from the seafloor.

FIGURE 3

Prokaryotic SSU rRNA gene phylotype compositions, as obtained by clone analysis in the waters from trench axis station E and continental and oceanic slope stations 2 and F, respectively, in the Japan Trench. Seawater samples from stations E, 2, and F were taken 76, 95, and 76 days after the Tohoku Earthquake on March 11, 2011, respectively. The numbers parentheses indicate the numbers of sequences obtained from each clone library.

FIGURE 4

Result of running Jackknife Environment Clusters of the SSU rRNA gene clone libraries obtained from the waters in the Japan Trench. Nodes recovered 99.9% of the time are red, 90–99.9% are orange, 70–90% are green, and <50% are blue.

FIGURE 5

Relative abundance of the amoA gene groups throughout the water column, as estimated by quantitative PCR in the Japan Trench region. The classification of the archaeal amoA subgroups is shown in Supplementary Figure S8. Water samples from the deepest depth for each station were taken at above 10 m from the seafloor. Green, blue, light blue, and orange indicate relative abundance of archaeal amoA groups A, Ba, Bb, and C/D, and light green indicate betaproteobacterial amoA.