Abstract

Hadal ocean sediments, found at sites deeper than 6,000 m water depth, are thought to contain microbial communities distinct from those at shallower depths due to high hydrostatic pressures and higher abundances of organic matter. These communities may also differ from one other as a result of geographical isolation. Here we compare microbial community composition in surficial sediments of two hadal environments—the Mariana and Kermadec trenches—to evaluate microbial biogeography at hadal depths. Sediment microbial consortia were distinct between trenches, with higher relative sequence abundances of taxa previously correlated with organic matter degradation present in the Kermadec Trench. In contrast, the Mariana Trench, and deeper sediments in both trenches, were enriched in taxa predicted to break down recalcitrant material and contained other uncharacterized lineages. At the 97% similarity level, sequence-abundant taxa were not trench-specific and were related to those found in other hadal and abyssal habitats, indicating potential connectivity between geographically isolated sediments. Despite the diversity of microorganisms identified using culture-independent techniques, most isolates obtained under in situ pressures were related to previously identified piezophiles. Members related to these same taxa also became dominant community members when native sediments were incubated under static, long-term, unamended high-pressure conditions. Our results support the hypothesis that there is connectivity between sediment microbial populations inhabiting the Mariana and Kermadec trenches while showing that both whole communities and specific microbial lineages vary between trench of collection and sediment horizon depth. This in situ biodiversity is largely missed when incubating samples within pressure vessels and highlights the need for revised protocols for high-pressure incubations.

Highlights

  • Ocean sediments make up one of the largest biomes on earth, harboring an estimated 3 × 1029 total microbial cells distributed in 3 × 108 km3 of sediment with 8 × 107 km3 of pore water (Kallmeyer et al, 2012; Amend and LaRowe, 2016)

  • We investigated the microbial communities within surficial sediment (0–10 cm) samples collected from 6- to 9-km water depths in the Kermadec Trench and 7- to 8-km depths in the Mariana Trench with both culture-independent high-throughput 16S rRNA gene sequencing and culture-dependent characterization

  • These shared operational taxonomic units (OTUs) included members related to the Marine Group I (MGI) within the Thaumarchaeota, the JTB255 clade and the genus Marinicella within the Gammaproteobacteria, the Rhodobacterales and Rhodospirillales within the Alphaproteobacteria, the class JTB23 within the Proteobacteria, and BD2–11 within the Gemmatimonadetes (Figure 2, Supplementary Table 2)

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Summary

Introduction

Ocean sediments make up one of the largest biomes on earth, harboring an estimated 3 × 1029 total microbial cells distributed in 3 × 108 km of sediment with 8 × 107 km of pore water (Kallmeyer et al, 2012; Amend and LaRowe, 2016). While surficial sediments include high abundances of Gammaproteobacteria, Deltaproteobacteria, Alphaproteobacteria, and Actinobacteria (Zinger et al, 2011; Ruff et al, 2015), deeper subsurface layers are dominated by the Chloroflexi and Atribacteria (OP9/JS1; Bienhold et al, 2016; Walsh et al, 2016b). These deeper communities may consist of taxa adapted to deep subsurface conditions (Inagaki et al, 2015) or which are found at shallower sediment horizon depths and survive after burial (Starnawski et al, 2017). Highpressure, culture-based analyses have predominantly found copiotrophic members of the Gammaproteobacteria, including Shewanella, Colwellia, Moritella, and Psychromonas (Kato et al, 1998; Nogi et al, 1998, 2002, 2004, 2007)

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