Microbial community stratification controlled by the subseafloor fluid flow and geothermal gradient at the Iheya North hydrothermal field in the Mid-Okinawa Trough (Integrated Ocean Drilling Program Expedition 331)

Abstract

The impacts of lithologic structure and geothermal gradient on subseafloor microbial communities were investigated at a marginal site of the Iheya North hydrothermal field in the Mid-Okinawa Trough. Subsurface marine sediments composed of hemipelagic muds and volcaniclastic deposits were recovered through a depth of 151 m below the seafloor at site C0017 during Integrated Ocean Drilling Program Expedition 331. Microbial communities inferred from 16S rRNA gene clone sequencing in low-temperature hemipelagic sediments were mainly composed of members of the Chloroflexi and deep-sea archaeal group. In contrast, 16S rRNA gene sequences of marine group I Thaumarchaeota dominated the microbial phylotype communities in the coarse-grained pumiceous gravels interbedded between the hemipelagic sediments. Based on the physical properties of sediments such as temperature and permeability, the porewater chemistry, and the microbial phylotype compositions, the shift in the physical properties of the sediments is suggested to induce a potential subseafloor recharging flow of oxygenated seawater in the permeable zone, leading to the generation of variable chemical environments and microbial communities in the subseafloor habitats. In addition, the deepest section of sediments under high-temperature conditions (∼90°C) harbored the sequences of an uncultivated archaeal lineage of hot water crenarchaeotic group IV that may be associated with the high-temperature hydrothermal fluid flow. These results indicate that the subseafloor microbial community compositions and functions at the marginal site of the hydrothermal field are highly affected by the complex fluid flow structure, such as recharging seawater and underlying hydrothermal fluids, coupled with the lithologic transition of sediments.

FIG 1

Temperature profile (A), lithostratigraphic transition (B), and core photograph (C) of sediment samples at IODP expedition 331 site C0017, which were originally published elsewhere (26). The black diamonds indicate in situ temperature measured by the APCT-3 temperature shoe. The gray diamond indicates the exposed minimum temperature determined by a thermoseal strip taped to the outer surface of the core liner. The lithologic description was roughly modified to show the entire sedimentary structure of the core samples. The photographs were taken from the section closest to the microbiology samples used in the present study.

FIG 2

Depth profile of porewater alkalinity, the ammonium, nitrate, sulfate, and acetate concentrations and the carbon isotopic composition of acetate in the core samples at site C0017. The original data regarding alkalinity, ammonium, nitrate, and sulfate were published elsewhere (26).

FIG 3

Total cell counts and numbers of 16S rRNA and functional genes in the subseafloor core samples at site C0017. (A) Total cell counts (open circles) and the 16S rRNA gene numbers of prokaryotes (black circles), bacteria (dark gray triangles), and archaea (light gray diamonds) quantified by Q-PCR. The total cell counts were originally reported by Takai et al. (26). (B) Numbers of functional genes dsrA (dark gray triangles) and aprA (open squares).

FIG 4

16S rRNA gene phylotype compositions in the sediments at site C0017. The 16S rRNA gene fragments were amplified with the universal and archaeon-specific primer sets of Uni530F-907R and Arc530F-Arc958R, respectively. The numbers in parentheses indicate the number of clones.

FIG 5

Jackknife environment cluster analysis (A) and PCA (B) in the UniFrac program. The jackknife values were estimated using 100 permutations and are shown in the nodes of the dendrogram. Each axis of the PCA plot indicates the fraction of the variance in the data. The black circles, plus signs, and triangles indicate the sediment samples of units I, II, and III, respectively.