Ultra-small cells and DPANN genome unveiled inside an extinct vent chimney

AbstractChemosynthetic organisms flourish around deep-sea hydrothermal vents where energy-rich fluids are emitted from metal sulfide chimneys. In contrast to actively venting chimneys, the nature of microbial life in extinct chimneys without fluid venting remains largely unknown. Here, the occurrence of ultra-small cells in silica-filled grain boundaries inside an extinct chimney is demonstrated by high-resolution bio-signature mapping. The ultra-small cells are associated with extracellularly precipitated Cu2O nanocrystals. Single-gene analysis shows that the chimney interior is dominated by a member of Pacearchaeota known as a major phylum of DPANN. Genome-resolved metagenomic analysis reveals that the chimney Pacearchaeota member is equipped with a nearly full set of genes for fermentation-based energy generation from nucleic acids, in contrast to previously characterized Pacearchaeota members lacking many genes for nucleic acid fermentation. We infer that the ultra-small cells associated with silica and extracellular Cu2O nanocrystals in the grain boundaries are Pacearchaeota, on the basis of the experimentally demonstrated capability of silica to concentrate nucleic acids from seawater and the presence of Cu-exporting genes in a reconstructed Pacearchaeota genome. Given the existence of ~3-billion-year-old submarine hydrothermally deposited silica, proliferation of microbial life using silica-bound nucleic acids might be relevant to the primitive vent biosphere.

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Sulfide Ameliorates Metal Toxicity for Deep-Sea Hydrothermal Vent Archaea

Applied and Environmental Microbiology ◽

10.1128/aem.70.4.2551-2555.2004 ◽

2004 ◽

Vol 70 (4) ◽

pp. 2551-2555 ◽

Cited By ~ 37

Author(s):

Virginia P. Edgcomb ◽

Stephen J. Molyneaux ◽

Mak A. Saito ◽

Karen Lloyd ◽

Simone Böer ◽

...

Keyword(s):

Heavy Metals ◽

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Metal Sulfide ◽

Toxic Metal ◽

Stress Factors ◽

Microbial Life ◽

High Concentrations ◽

Free Metal

ABSTRACT The chemical stress factors for microbial life at deep-sea hydrothermal vents include high concentrations of heavy metals and sulfide. Three hyperthermophilic vent archaea, the sulfur-reducing heterotrophs Thermococcus fumicolans and Pyrococcus strain GB-D and the chemolithoautotrophic methanogen Methanocaldococcus jannaschii, were tested for survival tolerance to heavy metals (Zn, Co, and Cu) and sulfide. The sulfide addition consistently ameliorated the high toxicity of free metal cations by the formation of dissolved metal-sulfide complexes as well as solid precipitates. Thus, chemical speciation of heavy metals with sulfide allows hydrothermal vent archaea to tolerate otherwise toxic metal concentrations in their natural environment.

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Faculty Opinions recommendation of Larvae from afar colonize deep-sea hydrothermal vents after a catastrophic eruption.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.3582961.3290061 ◽

2010 ◽

Author(s):

Gretchen Hofmann ◽

Pauline C Yu

Keyword(s):

Deep Sea ◽

Hydrothermal Vents

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Trophic influences of metal accumulation in natural pollution laboratories at deep-sea hydrothermal vents of the Mid-Atlantic Ridge

The Science of The Total Environment ◽

10.1016/j.scitotenv.2006.12.022 ◽

2007 ◽

Vol 373 (2-3) ◽

pp. 464-472 ◽

Cited By ~ 30

Author(s):

Enikõ Kádár ◽

Valentina Costa ◽

Michel Segonzac

Keyword(s):

Deep Sea ◽

Hydrothermal Vents ◽

Metal Accumulation ◽

Mid Atlantic Ridge

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The microbiology of deep-sea hydrothermal vents

Journal of Experimental Marine Biology and Ecology ◽

10.1016/s0022-0981(96)90038-6 ◽

1996 ◽

Vol 196 (1-2) ◽

pp. 378-380

Author(s):

Barry Cragg

Keyword(s):

Deep Sea ◽

Hydrothermal Vents

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Nematode succession at deep-sea hydrothermal vents after a recent volcanic eruption with the description of two dominant species

Organisms Diversity & Evolution ◽

10.1007/s13127-012-0122-2 ◽

2013 ◽

Vol 13 (3) ◽

pp. 349-371 ◽

Cited By ~ 14

Author(s):

Sabine Gollner ◽

Maria Miljutina ◽

Monika Bright

Keyword(s):

Deep Sea ◽

Volcanic Eruption ◽

Hydrothermal Vents ◽

Dominant Species

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Growth and Phylogenetic Properties of Novel Bacteria Belonging to the Epsilon Subdivision of the Proteobacteria Enriched fromAlvinella pompejana and Deep-Sea Hydrothermal Vents

Applied and Environmental Microbiology ◽

10.1128/aem.67.10.4566-4572.2001 ◽

2001 ◽

Vol 67 (10) ◽

pp. 4566-4572 ◽

Cited By ~ 102

Author(s):

Barbara J. Campbell ◽

Christian Jeanthon ◽

Joel E. Kostka ◽

George W. Luther ◽

S. Craig Cary

Keyword(s):

Deep Sea ◽

Hydrothermal Vent ◽

Hydrothermal Vents ◽

Heterotrophic Bacteria ◽

Geographic Location ◽

Optimal Growth ◽

Small Subunit ◽

Ribosomal Gene ◽

Moderately Thermophilic ◽

Novel Bacteria

ABSTRACT Recent molecular characterizations of microbial communities from deep-sea hydrothermal sites indicate the predominance of bacteria belonging to the epsilon subdivision of Proteobacteria(epsilon Proteobacteria). Here, we report the first enrichments and characterizations of four epsilonProteobacteria that are directly associated withAlvinella pompejana, a deep sea hydrothermal vent polychete, or with hydrothermal vent chimney samples. These novel bacteria were moderately thermophilic sulfur-reducing heterotrophs growing on formate as the energy and carbon source. In addition, two of them (Am-H and Ex-18.2) could grow on sulfur lithoautrotrophically using hydrogen as the electron donor. Optimal growth temperatures of the bacteria ranged from 41 to 45°C. Phylogenetic analysis of the small-subunit ribosomal gene of the two heterotrophic bacteria demonstrated 95% similarity to Sulfurospirillum arcachonense, an epsilon Proteobacteria isolated from an oxidized marine surface sediment. The autotrophic bacteria grouped within a deeply branching clade of the epsilonProteobacteria, to date composed only of uncultured bacteria detected in a sample from a hydrothermal vent along the mid-Atlantic ridge. A molecular survey of various hydrothermal vent environments demonstrated the presence of two of these bacteria (Am-N and Am-H) in more than one geographic location and habitat. These results suggest that certain epsilonProteobacteria likely fill important niches in the environmental habitats of deep-sea hydrothermal vents, where they contribute to overall carbon and sulfur cycling at moderate thermophilic temperatures.

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Deep-sea ophiuroids (Echinodermata) from reducing and non-reducing environments in the North Atlantic Ocean

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315405011318h ◽

2005 ◽

Vol 85 (2) ◽

pp. 383-402 ◽

Cited By ~ 27

Author(s):

Sabine Stöhr ◽

Michel Segonzac

Keyword(s):

South Carolina ◽

Gulf Of Mexico ◽

Deep Sea ◽

Hydrothermal Vents ◽

Cold Seep ◽

Chemical Compositions ◽

Cold Seeps ◽

Additional Species ◽

Blake Ridge ◽

Reducing Environment

The animal communities associated with the deep-sea reducing environment have been studied for almost 30 years, but until now only a single species of ophiuroid, Ophioctenella acies, has been found at both hydrothermal vents and methane cold seeps. Since the faunal overlap between vent and seep communities is small and many endemic species have been found among other taxa (e.g. Mollusca, Crustacea), additional species of ophiuroids were expected at previously unstudied sites. Chemical compositions at reducing sites differ greatly from the nearby bathyal environment. Generally, species adapted to chemosynthetic environments are not found in non-chemosynthetic habitats, but occasional visitors of other bathyal species to vent and seep sites have been recorded among many taxa except ophiuroids. This paper presents an analysis of the ophiuroid fauna found at hydrothermal vents and non-reducing nearby sites on the Mid-Atlantic Ridge and on methane cold seeps in the Gulf of Mexico, at Blake Ridge off South Carolina and south of Barbados. In addition to O. acies, four species were found at vents, Ophiactis tyleri sp. nov., Ophiocten centobi, Ophiomitra spinea and Ophiotreta valenciennesi rufescens. While Ophioctenella acies appears to be restricted to chemosynthetic areas, the other four species were also found in other bathyal habitats. They also occur in low numbers (mostly single individuals), whereas species adapted to hydrothermal areas typically occur in large numbers. Ophioscolex tripapillatus sp. nov. and Ophiophyllum atlanticum sp. nov. are described from nearby non-chemosynthetic sites. In a cold seep south of Barbados, three species of ophiuroids were found, including Ophioctenella acies, Amphiura sp., Ophiacantha longispina sp. nov. and Ophioplinthaca chelys. From the cold seeps at Blake Ridge and the Gulf of Mexico, Ophienigma spinilimbatum gen. et sp. nov. is described, likely restricted to the reducing environment. Ophiotreta valenciennesi rufescens occurred abundantly among Lophelia corals in the Gulf of Mexico seeps, which is the first record of this species from the West Atlantic. Habitat descriptions complement the taxonomic considerations, and the distribution of the animals in reducing environments is discussed.

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Pressure and Temperature Adaptation of Cytosolic Malate Dehydrogenases of Shallowand Deep-Living Marine Invertebrates: Evidence for High Body Temperatures in Hydrothermal Vent Animals

Journal of Experimental Biology ◽

10.1242/jeb.159.1.473 ◽

1991 ◽

Vol 159 (1) ◽

pp. 473-487 ◽

Cited By ~ 2

Author(s):

ELIZABETH DAHLHOFF ◽

GEORGE N. SOMERO

Keyword(s):

Deep Sea ◽

Hydrothermal Vents ◽

Elevated Temperatures ◽

Marine Invertebrates ◽

Distribution Patterns ◽

Pressure Effects ◽

Temperature Adaptation ◽

Body Temperatures ◽

Elevated Pressures

Effects of temperature and hydrostatic pressure were measured on cytosolic malate dehydrogenases (cMDHs) from muscle tissue of a variety of shallow- and deep-living benthic marine invertebrates, including seven species endemic to the deep-sea hydrothermal vents. The apparent Michaelis-Menten constant (Km) of coenzyme (nicotinamide adenine dinucleotide, NADH), used to index temperature and pressure effects, was conserved within a narrow range (approximately 15–25 μmoll−1) at physiological temperatures and pressures for all species. However, at elevated pressures, the Km of NADH rose sharply for cMDHs of shallow species (depths of occurrence >Approximately 500 m), but not for the cMDHs of deep-sea species. Cytosolic MDHs of invertebrates from the deep-sea hydrothermal vents generally were not perturbed by elevated temperatures (15–25°C) at in situ pressures, but cMDHs of cold-adapted deep-sea species were. At a single measurement temperature, the Km of NADH for cMDHs from invertebrates from habitats with well-characterized temperatures was inversely related to maximal sustained body temperature. This correlation was used to predict the maximal sustained body temperatures of vent invertebrates for which maximal habitat and body temperatures are difficult to estimate. Species occurring on the ‘smoker chimneys’, which emit waters with temperatures up to 380°C, are predicted to have sustained body temperatures that are approximately 20–25°C higher than vent species living in cooler vent microhabitats. We conclude that, just as adaptation of enzymes to elevated pressures is important in establishing species’ depth distribution patterns, adaptation of pressure-adapted enzymes to temperature is critical in enabling certain vent species to exploit warm-water microhabitats in the vent environment.

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