Vertically distinct microbial communities in the Mariana and Kermadec trenches

Abstract

Hadal trenches, oceanic locations deeper than 6,000 m, are thought to have distinct microbial communities compared to those at shallower depths due to high hydrostatic pressures, topographical funneling of organic matter, and biogeographical isolation. Here we evaluate the hypothesis that hadal trenches contain unique microbial biodiversity through analyses of the communities present in the bottom waters of the Kermadec and Mariana trenches. Estimates of microbial protein production indicate active populations under in situ hydrostatic pressures and increasing adaptation to pressure with depth. Depth, trench of collection, and size fraction are important drivers of microbial community structure. Many putative hadal bathytypes, such as members related to the Marinimicrobia, Rhodobacteraceae, Rhodospirilliceae, and Aquibacter, are similar to members identified in other trenches. Most of the differences between the two trench microbiomes consists of taxa belonging to the Gammaproteobacteria whose distributions extend throughout the water column. Growth and survival estimates of representative isolates of these taxa under deep-sea conditions suggest that some members may descend from shallower depths and exist as a potentially inactive fraction of the hadal zone. We conclude that the distinct pelagic communities residing in these two trenches, and perhaps by extension other trenches, reflect both cosmopolitan hadal bathytypes and ubiquitous genera found throughout the water column.

Fig 1. Sample collection locations.

Pelagic sample collection locations within the Kermadec and Mariana trenches.

Fig 2. Microbial activity as a function of pressure using HPG.

A; Ratio of the percentage of active cells under in situ pressure versus atmospheric pressure. B; Ratio of the percentage of active cells at 110 MPa versus in situ pressure. Filled circles, seawater collected at <13°C, excluding the surface sample; open circles, seawater collected at >15°C.

Fig 3. Abundant pelagic phyla.

Relative abundances of the ten most abundant phyla in the pelagic zones of the Kermadec and Mariana trenches, organized by trench and size fraction (>3.0, 3.0–0.2, 0.2–0.1 μm).

Fig 4. Ordinations of sequenced abyssal and hadal communities.

Distances between abyssal and hadal communities visualized via ordinations using Bray-Curtis dissimilarity. A, Mariana Trench; B, Kermadec Trench; C, both trenches.

Fig 5. OTUs enriched in the hado- or abysso- pelagic communities.

A; OTUs showing enrichment within the hadal or abyssal zones of the Mariana and Kermadec trenches labeled by the lowest discernible taxonomic rank. Filled, enriched in the abyssal zone; open, enriched in the hadal zone. B; OTUs showing enrichment within the hadal zone of the Kermadec or Mariana trench. Filled, enriched in the Kermadec Trench; open, enriched in the Mariana Trench.

Fig 6. Isolates and their abundances.

A; Relative abundances of cultured isolates from seawater in the Kermadec and Mariana trenches at 0.1 MPa and 4°C on plates (n = 170) or in bulbs (n = 31). B; Combined relative abundances of OTUs similar to piezophilic Colwellia, Shewanella, Moritella, or Psychromonas species derived from the community data. C; Combined relative abundances of OTUs related to the genera Pseudoalteromonas, Pseudomonas, Psychrobacter, Halomonas, Shewanella, and Vibrio derived from the community data.