Deep subsurface life from North Pond: Enrichment, isolation, characterization and genomes of heterotrophic bacteria

Russell, Joseph A.; Leon-Zayas, Rosa; Wrighton, Kelly; Biddle, Jennifer F.

doi:10.3389/fmicb.2016.00678

Title: Deep subsurface life from North Pond: Enrichment, isolation, characterization and genomes of heterotrophic bacteria

Journal Article · Tue May 10 00:00:00 EDT 2016 · Frontiers in Microbiology

DOI: https://doi.org/10.3389/fmicb.2016.00678 · OSTI ID:1258445

Russell, Joseph A. ^[1]; Leon-Zayas, Rosa ^[1]; Wrighton, Kelly ^[2]; Biddle, Jennifer F. ^[1]

Univ. of Delaware, Lewes, DE, (United States)
The Ohio State Univ., Columbus, OH (United States)

Studies of subsurface microorganisms have yielded few environmentally relevant isolates for laboratory studies. In order to address this lack of cultivated microorganisms, we initiated several enrichments on sediment and underlying basalt samples from North Pond, a sediment basin ringed by basalt outcrops underlying an oligotrophic watercolumn west of the Mid-Atlantic Ridge at 22° N. In contrast to anoxic enrichments, growth was observed in aerobic, heterotrophic enrichments from sediment of IODP Hole U1382B at 4 and 68 m below seafloor (mbsf). These sediment depths, respectively, correspond to the fringes of oxygen penetration from overlying seawater in the top of the sediment column and upward migration of oxygen from oxic seawater from the basalt aquifer below the sediment. Here we report the enrichment, isolation, initial characterization and genomes of three isolated aerobic heterotrophs from North Pond sediments; an Arthrobacter species from 4 mbsf, and Paracoccus and Pseudomonas species from 68 mbsf. These cultivated bacteria are represented in the amplicon 16S rRNA gene libraries created from whole sediments, albeit at low (up to 2%) relative abundance. We provide genomic evidence from our isolates demonstrating that the Arthrobacter and Pseudomonas isolates have the potential to respire nitrate and oxygen, though dissimilatory nitrate reduction could not be confirmed in laboratory cultures. Furthermore, the cultures from this study represent members of abundant phyla, as determined by amplicon sequencing of environmental DNA extracts, and allow for further studies into geochemical factors impacting life in the deep subsurface.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1258445

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 7; ISSN 1664-302X

Publisher:: Frontiers Research FoundationCopyright Statement

Country of Publication:: United States

Language:: English

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Evidence for Direct Electron Transfer by a Gram-Positive Bacterium Isolated from a Microbial Fuel Cell Wrighton, K. C.; Thrash, J. C.; Melnyk, R. A. Applied and Environmental Microbiology, Vol. 77, Issue 21 https://doi.org/10.1128/AEM.05365-11	journal	September 2011
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Growth Pattern and Yield of a Chemoautotrophic Beggiatoa sp. in Oxygen-Sulfide Microgradients Nelson, Douglas C.; Jørgensen, Bo Barker; Revsbech, Niels Peter Applied and Environmental Microbiology, Vol. 52, Issue 2 https://doi.org/10.1128/AEM.52.2.225-233.1986	journal	January 1986
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cumA, a Gene Encoding a Multicopper Oxidase, Is Involved in Mn2+ Oxidation in Pseudomonas putida GB-1 Brouwers, Geert-Jan; de Vrind, Johannes P. M.; Corstjens, Paul L. A. M. Applied and Environmental Microbiology, Vol. 65, Issue 4 https://doi.org/10.1128/AEM.65.4.1762-1768.1999	journal	April 1999
High-Throughput Methods for Culturing Microorganisms in Very-Low-Nutrient Media Yield Diverse New Marine Isolates Connon, S. A.; Giovannoni, S. J. Applied and Environmental Microbiology, Vol. 68, Issue 8 https://doi.org/10.1128/AEM.68.8.3878-3885.2002	journal	August 2002
Isolation of a Methanogen from Deep Marine Sediments That Contain Methane Hydrates, and Description of Methanoculleus submarinus sp. nov Mikucki, Jill A.; Liu, Yitai; Delwiche, Mark Applied and Environmental Microbiology, Vol. 69, Issue 6 https://doi.org/10.1128/AEM.69.6.3311-3316.2003	journal	June 2003
Mercury Adaptation among Bacteria from a Deep-Sea Hydrothermal Vent Vetriani, Costantino; Chew, Yein S.; Miller, Susan M. Applied and Environmental Microbiology, Vol. 71, Issue 1 https://doi.org/10.1128/AEM.71.1.220-226.2005	journal	January 2005
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Genomic Insights into Mn(II) Oxidation by the Marine Alphaproteobacterium Aurantimonas sp. Strain SI85-9A1 Dick, G. J.; Podell, S.; Johnson, H. A. Applied and Environmental Microbiology, Vol. 74, Issue 9 https://doi.org/10.1128/aem.01656-07	journal	March 2008
Isolation of a Methanogen from Deep Marine Sediments That Contain Methane Hydrates, and Description of Methanoculleus submarinus sp. nov Mikucki, Jill A.; Liu, Yitai; Delwiche, Mark Applied and Environmental Microbiology, Vol. 69, Issue 6 https://doi.org/10.1128/aem.69.6.3311-3316.2003	journal	June 2003
Mercury Adaptation among Bacteria from a Deep-Sea Hydrothermal Vent Vetriani, Costantino; Chew, Yein S.; Miller, Susan M. Applied and Environmental Microbiology, Vol. 71, Issue 1 https://doi.org/10.1128/aem.71.1.220-226.2005	journal	January 2005
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Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditionsThis article is one of a selection of papers in the Special Issue on Polar and Alpine Microbiology. Marx, Joseph G.; Carpenter, Shelly D.; Deming, Jody W. Canadian Journal of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1139/W08-130	journal	January 2009
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Production of cryoprotectant extracellular polysaccharide substances (EPS) by the marine psychrophilic bacterium Colwellia psychrerythraea strain 34H under extreme conditionsThis article is one of a selection of papers in the Special Issue on Polar and Alpine Microbiology. Marx, Joseph G.; Carpenter, Shelly D.; Deming, Jody W. Canadian Journal of Microbiology, Vol. 55, Issue 1 https://doi.org/10.1139/w08-130	journal	January 2009
The Deep, Dark Energy Biosphere: Intraterrestrial Life on Earth Edwards, Katrina J.; Becker, Keir; Colwell, Frederick Annual Review of Earth and Planetary Sciences, Vol. 40, Issue 1 https://doi.org/10.1146/annurev-earth-042711-105500	journal	May 2012
Measurement of in Situ Activities of Nonphotosynthetic Microorganisms in Aquatic and Terrestrial Habitats Staley, J. T.; Konopka, A. Annual Review of Microbiology, Vol. 39, Issue 1 https://doi.org/10.1146/annurev.mi.39.100185.001541	journal	October 1985
Predicting active site residue annotations in the Pfam database Mistry, Jaina; Bateman, Alex; Finn, Robert D. BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-298	journal	August 2007
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Reagent and laboratory contamination can critically impact sequence-based microbiome analyses Salter, Susannah J.; Cox, Michael J.; Turek, Elena M. BMC Biology, Vol. 12, Issue 1 https://doi.org/10.1186/s12915-014-0087-z	journal	November 2014
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Evidence for Microbial Carbon and Sulfur Cycling in Deeply Buried Ridge Flank Basalt C., Shanks, Wayne; Kai-Uwe, Hinrichs,; A., Lever, Mark The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/6v0c-wx70	text	January 2013
Reagent and laboratory contamination can critically impact sequence-based microbiome analyses. Salter, Susannah; Cox, Michael J.; Turek, Elena M. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.41109	text	January 2014
An inter-laboratory study to investigate the impact of the bioinformatics component on microbiome analysis using mock communities. O'Sullivan, Denise M.; Doyle, Ronan M.; Temisak, Sasithon Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.71609	text	January 2021
Initiation of long-term coupled microbiological, geochemical, and hydrological experimentation within the seafloor at North Pond, western flank of the Mid-Atlantic Ridge Integrated Ocean Drilling Program Expedition 336 Preliminary Report https://doi.org/10.2204/iodp.pr.336.2012	book	September 2011
Enrichment and Cultivation of Microorganisms from Sediment from the Slope of the Peru Trench (ODP Site 1230) Biddle, Jennifer F.; House, Christopher H.; Brenchley, Jean E. Proceedings of the Ocean Drilling Program, 201 Scientific Results https://doi.org/10.2973/odp.proc.sr.201.107.2005	book	June 2005
Linking microbial heterotrophic activity and sediment lithology in oxic, oligotrophic sub-seafloor sediments of the North Atlantic Ocean Frontiers in Microbiology https://doi.org/10.3389/fmicb.2011.00263	journal	January 2011
Isolation of Sulfate-Reducing Bacteria from Sediments Above the Deep-Subseafloor Aquifer Fichtel, Katja; Mathes, Falko; Könneke, Martin Frontiers in Microbiology, Vol. 3 https://doi.org/10.3389/fmicb.2012.00065	journal	January 2012
Nitrogen cycling in the deep sedimentary biosphere: nitrate isotopes in porewaters underlying the oligotrophic North Atlantic Wankel, S. D.; Buchwald, C.; Ziebis, W. Biogeosciences, Vol. 12, Issue 24 https://doi.org/10.5194/bg-12-7483-2015	journal	January 2015

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BusyBee Web: metagenomic data analysis by bootstrapped supervised binning and annotation Laczny, Cedric C.; Kiefer, Christina; Galata, Valentina Nucleic Acids Research, Vol. 45, Issue W1 https://doi.org/10.1093/nar/gkx348	journal	May 2017
Cytosine methylation within marine sediment microbial communities: potential epigenetic adaptation to the environment Rambo, Ian M.; Marsh, Adam; Biddle, Jennifer F. bioRxiv https://doi.org/10.1101/167189	journal	July 2017
Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time Bradley, James A.; Amend, Jan P.; LaRowe, Douglas E. Geobiology, Vol. 17, Issue 1 https://doi.org/10.1111/gbi.12313	journal	September 2018
Complete Genome Sequence of Bacillus subtilis Strain 29R7-12, a Piezophilic Bacterium Isolated from Coal-Bearing Sediment 2.4 Kilometers below the Seafloor Wei, Yuli; Cao, Junwei; Fang, Jiasong Genome Announcements, Vol. 5, Issue 8 https://doi.org/10.1128/genomea.01621-16	journal	February 2017
Predominance of Viable Spore-Forming Piezophilic Bacteria in High-Pressure Enrichment Cultures from ~1.5 to 2.4 km-Deep Coal-Bearing Sediments below the Ocean Floor Fang, Jiasong; Kato, Chiaki; Runko, Gabriella M. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00137	journal	February 2017
Ecology and evolution of seafloor and subseafloor microbial communities Orsi, William D. Nature Reviews Microbiology, Vol. 16, Issue 11 https://doi.org/10.1038/s41579-018-0046-8	journal	July 2018
Survival of the fewest: Microbial dormancy and maintenance in marine sediments through deep time Bradley, James A.; Amend, Jan P.; LaRowe, Douglas E. Geobiology, Vol. 17, Issue 1 https://doi.org/10.1111/gbi.12313	journal	September 2018

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