Hydraulically Fractured Natural-Gas Well Microbial Communities Contain Genomic Halogenation and Dehalogenation Potential

Organohalides
are routinely detected in fluid produced from hydraulically
fractured oil and natural-gas wells, yet the origin and fate of these
compounds remain largely unknown. Because few organohalides are disclosed
as fracturing fluid additives, one suspected formation mechanism is
the reaction of geogenic halides oxidized by injected additives with
natural or anthropogenic organic carbon. However, the potential role
of microorganisms in organohalide cycling is currently unknown. Here,
we uncover the microorganisms and enzymatic systems that contribute
to organohalide transformations during hydraulic fracturing through
nontarget organohalide chemical analysis and metagenomics. Twenty
organohalide compounds were identified in fluid samples produced from
two Marcellus Shale natural-gas wells, comprising five structural
classes. Genes encoding halogenation and dehalogenation mechanisms
were identified in metagenomes assembled from produced fluids collected
from four Appalachian Basin natural-gas wells. Metagenomic results
show the presence of non-heme chloroperoxidases, enzymes that generate
peracetic acid, which can react with dissolved halides to form highly
oxidizing hypohalous acid, a halogenation agent for geogenic or anthropogenic
organic matter. Microbial organohalide transformation/mineralization
could proceed through hydrolytic dehalogenation, with enzymes inferred
to operate on haloacetates, haloacids, and haloalkanes of varying
carbon chain lengths, some of which are present in these wells. These
results indicate that microorganisms may play an underappreciated
role in direct and indirect organohalide transformations in hydraulically
fractured oil and gas systems.