Award: OCE-0961894

Scientific Merit. Every summer in many
estuaries and coastal margins, eutrophication-elevated phytoplankton production
drives rapid bacterial growth, which consumes oxygen and creates hypoxic and
anoxic bottom waters. These so-called “dead zones” exclude fish, kill benthic
organisms, and eliminate habitat. Despite their popular name, anoxic/hypoxic
zones are not really dead, but rather are populated with living and active
microbial communities. Once oxygen is depleted, microbes switch to anaerobic
metabolisms to respire organic matter, and they follow a succession based on
the energetics and availability of the compound they use in place of oxygen (e.g.,
O₂, NO₃^-, Mn(IV), Fe(III), and SO₄^2-).
Anaerobic respiration and anaerobic bacterial production had never been
measured simultaneously in the water column of seasonally anoxic estuarine
waters, and thus the impact of these zones on estuarine carbon cycles are
either unknown or approximated from indirect measurements (e.g., sulfate
respiration rate). Our
detailed surveys of anoxic bottom waters applied new techniques for measuring
bacterial growth, respiration, diversity, and gene expression to better
understand the Life in the Dead Zone. We mapped patterns in redox chemistry and
demonstrated parallel space-for-time development in which changes associated
with aging bottom waters as they moved up-estuary matched changes at a single
station over time. From April to October, redox conditions shifted from oxic to
hypoxic to sub-oxic to sulfidic, and then shifted back to oxic either gradually
(2010) or quickly (2011) following hurricane-associated mixing of the Bay. These
changes in redox chemistry paralleled changes in the phylogenetic diversity of
bacterial communities, in microbial gene expression patterns, and in
heterotrophic activity. Spatially, bottom waters moving up-estuary changed from
oxic to hypoxic to sub-oxic to sulfidic, with comparable shifts in phylogenetic
diversity and heterotrophic activity. A third formation of this coordinated
shift in redox chemistry and biology existed at the pycnocline/oxycline
overlying anoxic bottom waters. This gradient varied in thickness with
stratification strength, and was often thin and difficult to sample. Our
results suggest that this redox gradient hosts a gradient in microbial
diversity, heterotrophic activity, and thin layers of intense chemoautotrophic
metabolism. Thus, we identified spatial and temporal transitions between oxic
and sulfidic waters each of which hosted coordinated shifts in microbial
activity, diversity and gene expression. Biological communities were
surprisingly active under all redox states, including sulfidic waters where
somewhat reduced rates of heterotrophic production were paired with elevated
rates of chemoautotrophic production.

 

Broader Impacts. Estuaries are
centers of human population, and they provide society with innumerable
recreational and economic benefits. Recently, anoxic and hypoxic zones in
estuaries came to the public’s attention as indicators of anthropogenic
eutrophication. Anoxia/hypoxia is now considered a bellwether of eutrophication
in coastal waters, and consequently, most anoxia-related estuarine research is
aimed at managing the problem. In contrast, relatively little effort has gone
into studying the basic biogeochemistry, microbial ecology and diversity of
these waters and the impact of anaerobic respiration on estuarine ecosystems. This
research advanced estuarin...