Project: Life in the Dead Zone: Microbial respiration, production, diversity and gene expression in seasonally anoxic estuarine waters

Every summer in many estuaries and coastal margins, eutrophication-elevated phytoplankton production drives rapid bacterial respiration creating 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 very active microbial communities. In fact, bacterial production in anoxic waters can exceed that in overlying oxic waters due, in part, to reduced grazing and increased cell size and abundance. Once oxygen is depleted, microbial respiration undergoes a succession of redox reactions with decreasing energy yield as terminal electron acceptors are depleted (e.g., O2, NO3-, Mn(IV), Fe(III), and SO42-). This combination of high production and reduced growth efficiency creates a condition in which respiration may be very high, making anoxic zones significant sinks for organic matter and key sites for nutrient cycling.

Previous research documented respiratory succession in Chesapeake Bay bottom waters based on redox chemistry measurements. Heterotrophic bacterial production was very high at some stages of this succession, suggesting elevated respiration. Also, the phylogenetic composition of bacterioplankton communities in anoxic waters was similar to oxic surface waters for nearly half the summer, only changing after the appearance of H2S. This suggests that typical aerobic estuarine bacteria are able to shift to anaerobic metabolisms and continue to dominate.

Most of what is known about microbial respiration and community composition in anoxic water comes from studies of permanently anoxic systems like the Black Sea and Cariaco Basin. By comparison, very little is known about what is a much more common and more dynamic marine environment – seasonally anoxic estuarine waters. This proposal describes a 3-year integrated study to advance the quantitative and mechanistic understanding of biogeochemical cycling in one of the largest seasonal estuarine anoxic zones in the USA. It hypothesize that:

• Dominant sub-pycnocline respiratory processes undergo a succession from aerobic respiration to nitrate respiration and metal reduction to sulfate reduction.
• Bacterial growth efficiency decreases with this respiratory succession, but bacterial production remains high, resulting in very high carbon respiration rates.
• Bacterial community composition changes little during respiratory succession until sulfate respiration dominates (i.e., the sulfide threshold), but gene expression closely tracks changes in redox conditions in order to support the most energetic respiratory processes.

These hypotheses will be addressed by quantifying carbon respiration rates using several techniques including delta CO2; quantifying bacterial production, biomass and growth efficiency; and characterizing succession in the composition and respiratory gene expression patterns of microbial communities in water column and sediments during each stage of respiratory succession. This project will integrate biogeochemical, biological, and genomic data to explain how biogeochemistry influences, and is influenced by, microbial respiration, production, diversity, and gene expression.

The proposed research will provide (1) reliable measurements of production and respiration in anoxic/hypoxic waters, (2) techniques applicable to other ecosystems, and (3) ecological insight for predicting future changes with ongoing restoration efforts in anoxia-impacted estuaries. These measurements will be useful for calibrating biogeochemical models and for estimating carbon budgets. This research will train two graduate students and one postdoctoral scientist in several state-of-the-art geochemical and molecular biology techniques. Applications will be submitted to the NSF Research Experiences for Teachers program to engage two teachers to work on this project and to participate in the seven-week Environmental Science Education Partnership (ESEP) Teacher Research Fellowship Program (www.esep.umces.edu) at UMCES Horn Point Laboratory. New discoveries will be incorporated into graduate-level courses entitled Aquatic Microbial Ecology, Biological Oceanography, and Environmental Geochemistry. Nucleic acid sequences will be deposited in online repositories including GenBank.