CaltechAUTHORS
  A Caltech Library Service

Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments

Glass, Jennifer B. and Yu, Hang and Steele, Joshua A. and Dawson, Katherine S. and Sun, Shulei and Chourey, Karuna and Pan, Chongle and Hettich, Robert L. and Orphan, Victoria J. (2014) Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments. Environmental Microbiology, 16 (6). pp. 1592-1633. ISSN 1462-2912. http://resolver.caltech.edu/CaltechAUTHORS:20140717-091139174

[img]
Preview
PDF (Figure S1) - Supplemental Material
See Usage Policy.

245Kb
[img]
Preview
PDF (Figures S2) - Supplemental Material
See Usage Policy.

336Kb
[img]
Preview
PDF (Table S1) - Supplemental Material
See Usage Policy.

43Kb
[img]
Preview
PDF (Table S2) - Supplemental Material
See Usage Policy.

40Kb

Use this Persistent URL to link to this item: http://resolver.caltech.edu/CaltechAUTHORS:20140717-091139174

Abstract

Microbes have obligate requirements for trace metals in metalloenzymes that catalyse important biogeochemical reactions. In anoxic methane- and sulphide-rich environments, microbes may have unique adaptations for metal acquisition and utilization because of decreased bioavailability as a result of metal sulphide precipitation. However, micronutrient cycling is largely unexplored in cold (≤ 10°C) and sulphidic (> 1 mM ΣH_(2)S) deep-sea methane seep ecosystems. We investigated trace metal geochemistry and microbial metal utilization in methane seeps offshore Oregon and California, USA, and report dissolved concentrations of nickel (0.5–270 nM), cobalt (0.5–6 nM), molybdenum (10–5600 nM) and tungsten (0.3–8 nM) in Hydrate Ridge sediment porewaters. Despite low levels of cobalt and tungsten, metagenomic and metaproteomic data suggest that microbial consortia catalysing anaerobic oxidation of methane (AOM) utilize both scarce micronutrients in addition to nickel and molybdenum. Genetic machinery for cobalt-containing vitamin B_(12) biosynthesis was present in both anaerobic methanotrophic archaea (ANME) and sulphate-reducing bacteria. Proteins affiliated with the tungsten-containing form of formylmethanofuran dehydrogenase were expressed in ANME from two seep ecosystems, the first evidence for expression of a tungstoenzyme in psychrophilic microorganisms. Overall, our data suggest that AOM consortia use specialized biochemical strategies to overcome the challenges of metal availability in sulphidic environments.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1111/1462-2920.12314DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/1462-2920.12314/abstractPublisherArticle
ORCID:
AuthorORCID
Yu, Hang0000-0002-7600-1582
Dawson, Katherine S.0000-0001-8856-4609
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2013 Society for Applied Microbiology and John Wiley & Sons Ltd. Received 25 August, 2013; accepted 13 October, 2013. We thank Stephanie Connon, Nathan Dalleska, Varun Gadh, Alexis Pasulka, Annelie Pernthaler, Rachel Poretsky and Patricia Tavormina for technical assistance; Jess Adkins, Ken Farley, Lindsay Hedges, Guillaume Paris, and Alex Rider for assistance with ICP-MS analysis; Steve Bates, Anthony Chappaz, George Helz, Sebastian Kopf, Timothy Lyons, James Morgan, Silvan Scheller, Silke Severmann and Laura Wasylenki for helpful discussions; and Roland Hatzenpichler for manuscript comments. We are grateful to the captain, pilots, crew and shipboard research parties of the R/V Western Flyer and R/V Atlantis (AT-15–68 and AT-18-10) for their invaluable support. We also thank Bill Ussler III, Charlie Paull and Husen Zhang for assistance with sample collection from Santa Monica Basin in 2005. We also acknowledge the Gordon and Betty Moore Foundation, and Stephan Schuster for financial and technical support with sequencing BC3 and BC4 at Penn State. This work was supported by grants from the Department of Energy Division of Biological and Environmental Research (DE-SC0004949), the National Aeronautics and Space Administration Astrobiology Institute (Penn State Astrobiology Research Center), and the Gordon and Betty Moore Foundation and the National Science Foundation (OCE-0825791) to V.J.O. Samples from Eel River Basin and Hydrate Ridge were collected as part of NSF funded projects (MCB-0348492; OCE-0825791) to V.J.O. J.B.G. was supported by a National Aeronautics and Space Administration Astrobiology Postdoctoral Fellowship.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0004949
NASAUNSPECIFIED
Gordon and Betty Moore FoundationUNSPECIFIED
NSFOCE-0825791
NSFMCB-0348492
Record Number:CaltechAUTHORS:20140717-091139174
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140717-091139174
Official Citation:Glass, J. B., Yu, H., Steele, J. A., Dawson, K. S., Sun, S., Chourey, K. , Pan, C., Hettich, R. L. and Orphan, V. J. (2014), Geochemical, metagenomic and metaproteomic insights into trace metal utilization by methane-oxidizing microbial consortia in sulphidic marine sediments. Environmental Microbiology, 16: 1592–1611. doi: 10.1111/1462-2920.12314
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:47287
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:18 Jul 2014 19:38
Last Modified:20 Mar 2019 21:32

Repository Staff Only: item control page