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Title: Metatranscriptomic evidence of pervasive and diverse chemolithoautotrophy relevant to C, S, N and Fe cycling in a shallow alluvial aquifer

Journal Article · · The ISME Journal
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  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences

Groundwater ecosystems are conventionally thought to be fueled by surface-derived allochthonous organic matter and dominated by heterotrophic microbes living under often-oligotrophic conditions. However, in a 2-month study of nitrate amendment to a perennially suboxic aquifer in Rifle (CO), strain-resolved metatranscriptomic analysis revealed pervasive and diverse chemolithoautotrophic bacterial activity relevant to C, S, N and Fe cycling. Before nitrate injection, anaerobic ammonia-oxidizing (anammox) bacteria accounted for 16% of overall microbial community gene expression, whereas during the nitrate injection, two other groups of chemolithoautotrophic bacteria collectively accounted for 80% of the metatranscriptome: (1) members of the Fe(II)-oxidizing Gallionellaceae family and (2) strains of the S-oxidizing species, Sulfurimonas denitrificans. Notably, the proportion of the metatranscriptome accounted for by these three groups was considerably greater than the proportion of the metagenome coverage that they represented. Transcriptional analysis revealed some unexpected metabolic couplings, in particular, putative nitrate-dependent Fe(II) and S oxidation among nominally microaerophilic Gallionellaceae strains, including expression of periplasmic (NapAB) and membrane-bound (NarGHI) nitrate reductases. The three most active groups of chemolithoautotrophic bacteria in this study had overlapping metabolisms that allowed them to occupy different yet related metabolic niches throughout the study. Overall, these results highlight the important role that chemolithoautotrophy can have in aquifer biogeochemical cycling, a finding that has broad implications for understanding terrestrial carbon cycling and is supported by recent studies of geochemically diverse aquifers.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Inst. of Health (NIH) (United States)
Grant/Contract Number:
AC02-05CH11231; S10RR029668; S10RR027303
OSTI ID:
1377452
Journal Information:
The ISME Journal, Vol. 10, Issue 9; ISSN 1751-7362
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 73 works
Citation information provided by
Web of Science

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Hidden diversity revealed by genome-resolved metagenomics of iron-oxidizing microbial mats from Lō’ihi Seamount, Hawai’i journal April 2017
Thousands of microbial genomes shed light on interconnected biogeochemical processes in an aquifer system journal October 2016
High reactivity of deep biota under anthropogenic CO2 injection into basalt journal October 2017
H2S events in the Peruvian oxygen minimum zone facilitate enhanced dissolved Fe concentrations journal August 2018
Paired RNA Radiocarbon and Sequencing Analyses Indicate the Importance of Autotrophy in a Shallow Alluvial Aquifer journal July 2019
Microbial anaerobic Fe(II) oxidation - Ecology, mechanisms and environmental implications: Microbial anaerobic Fe(II) oxidation journal October 2018
Comparison of sulfide‐oxidizing Sulfurimonas strains reveals a new mode of thiosulfate formation in subsurface environments journal January 2020
Insights into Carbon Metabolism Provided by Fluorescence In Situ Hybridization-Secondary Ion Mass Spectrometry Imaging of an Autotrophic, Nitrate-Reducing, Fe(II)-Oxidizing Enrichment Culture journal March 2018
Growth and Population Dynamics of the Anaerobic Fe(II)-Oxidizing and Nitrate-Reducing Enrichment Culture KS journal March 2018
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