Microbial Ecology of the Dark Ocean above, at, and below the Seafloor

Abstract

SUMMARY The majority of life on Earth—notably, microbial life—occurs in places that do not receive sunlight, with the habitats of the oceans being the largest of these reservoirs. Sunlight penetrates only a few tens to hundreds of meters into the ocean, resulting in large-scale microbial ecosystems that function in the dark. Our knowledge of microbial processes in the dark ocean—the aphotic pelagic ocean, sediments, oceanic crust, hydrothermal vents, etc.—has increased substantially in recent decades. Studies that try to decipher the activity of microorganisms in the dark ocean, where we cannot easily observe them, are yielding paradigm-shifting discoveries that are fundamentally changing our understanding of the role of the dark ocean in the global Earth system and its biogeochemical cycles. New generations of researchers and experimental tools have emerged, in the last decade in particular, owing to dedicated research programs to explore the dark ocean biosphere. This review focuses on our current understanding of microbiology in the dark ocean, outlining salient features of various habitats and discussing known and still unexplored types of microbial metabolism and their consequences in global biogeochemical cycling. We also focus on patterns of microbial diversity in the dark ocean and on processes and communities that are characteristic of the different habitats.

Microorganisms persist at record depths in the subseafloor of the Canterbury Basin

“…Although in subsurface sediment shallower than 1000 m.b.sf. background molecular data on bacterial and archaeal lineages exists (for example, Inagaki et al, 2006;Orcutt et al, 2011), most deep-subsurface microorganisms detected so far were refractory to cultivation (Sass and Parkes, 2011). The diversity of deeply buried microorganisms remains untapped, as subseafloor prokaryotic culturability in most studies is o0.1% of all microscopically detected cells (D'Hondt et al, 2004).…”

“…), as revealed by molecular, metagenomic and metatranscriptomic studies (Lipp et al, 2008;Roussel et al, 2008;Biddle et al, 2011;Pawlowski et al, 2011;Orsi et al, 2013a). It harbors representatives from the three domains of life, for example, numerous endemic and/or as yet uncultured Archaea and Bacteria (for example, Inagaki et al, 2006;Orcutt et al, 2011), in addition to bacterial endospores (Lomstein et al, 2012), protists and fungi belonging to Eukarya (Schippers and Neretin, 2006;Edgcomb et al, 2011;Orsi et al, 2013a,b). Occurrence of capsid-encoding organisms has also been confirmed (Engelhardt et al, 2011).…”

Phylogeny and physiology of candidate phylum ‘Atribacteria’ (OP9/JS1) inferred from cultivation-independent genomics

“…BMC-mediated metabolism of sugar phosphates such as deoxyribose 5-phosphate by the 'Atribacteria', as suggested by Axen et al, (2014), could also have an important role in nutrient recycling in these environments. The capacity for syntrophic propionate catabolism predicted for the JS1-1 lineage points to an ecological role for the 'Atribacteria' in sediments in the 'dark ocean biosphere', especially those associated with methane hydrates, hydrocarbon seeps and on continental margins and shelves where this candidate phylum is often abundant (Orcutt et al, 2011;Parkes et al, 2014). Although the existing genomic coverage only scratches the surface of the diversity encompassed by this candidate phylum, we posit that primary and secondary fermentation and syntrophy may be a common catabolic theme among members of the 'Atribacteria'.…”

“…Based on these results, the marine sediment sister lineage was posited to represent a distinct candidate phylum called JS1 (Webster et al, 2004). A current synthesis of the available data suggests that JS1 is a characteristic denizen of subseafloor environments, and is particularly abundant in sediments associated with methane hydrates and hydrocarbon seeps, and on continental margins and shelves (Inagaki et al, 2006;Orcutt et al, 2011;Parkes et al, 2014). Sequences related to JS1 have also been detected in environments such as petroleum reservoirs (Pham et al, 2009;Kobayashi et al, 2012), hypersaline microbial mats (Harris et al, 2013), and landfill leachates (Liu et al, 2011).…”

Lrs14 transcriptional regulators influence biofilm formation and cell motility of Crenarchaea

“…Archaea form biofilms within many microbial ecosystems such as acid mine drainage sites, seafloor sediments or acidic hot springs mats (Baker and Banfield, 2003;Orcutt et al, 2011); Kozubal et al, 2012). Initial description of the archaeal biofilms were reported in the euryarchaeota Archaeoglobus fulgidus (Lapaglia and Hartzell, 1997) and in the bi-species biofilm of Pyrococcus furiosus and Methanopyrus kandlerii (Schopf et al, 2008).…”