Metabolic Roles of Uncultivated Bacterioplankton Lineages in the Northern Gulf of Mexico "Dead Zone".

J Cameron Thrash,Kiley W Seitz,Olivia U Mason,Nancy N Rabalais,Brett J Baker,Ben Temperton,Lauren E Gillies,Bernard Henrissat,Mary Ann Moran

doi:10.1128/mbio.01017-17

Abstract

ABSTRACTMarine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. One of the largest of these coastal dead zones occurs on the continental shelf of the northern Gulf of Mexico (nGOM), which results from eutrophication-enhanced bacterioplankton respiration and strong seasonal stratification. Previous research in this dead zone revealed the presence of multiple cosmopolitan bacterioplankton lineages that have eluded cultivation, and thus their metabolic roles in this ecosystem remain unknown. We used a coupled shotgun metagenomic and metatranscriptomic approach to determine the metabolic potential of Marine Group II Euryarchaeota, SAR406, and SAR202. We recovered multiple high-quality, nearly complete genomes from all three groups as well as candidate phyla usually associated with anoxic environments—Parcubacteria (OD1) and Peregrinibacteria. Two additional groups with putative assignments to ACD39 and PAUC34f supplement the metabolic contributions by uncultivated taxa. Our results indicate active metabolism in all groups, including prevalent aerobic respiration, with concurrent expression of genes for nitrate reduction in SAR406 and SAR202, and dissimilatory nitrite reduction to ammonia and sulfur reduction by SAR406. We also report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f. Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter.

Highlights

Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics
Consistent with previous reports of obligate fermentative metabolism by Parcubacteria and Peregrinibacteria [23, 30, 31, 48], we identified no respiratory pathways for these taxa (Fig. 5), and they trended toward greater abundances in the lowest DO samples (Fig. S7)
We define roles for Marine Group II Euryarchaeota (MGII), SAR406, SAR202, Bin 13, and Bins 50/48 as aerobic heterotrophs, we observed concurrent expression of genes associated with anaerobic metabolism in SAR406, SAR202, MGII, and Bins 50/48 (DNRA) in suboxic samples with the lowest measured DO concentrations

Summary

Introduction

Marine regions that have seasonal to long-term low dissolved oxygen (DO) concentrations, sometimes called “dead zones,” are increasing in number and severity around the globe with deleterious effects on ecology and economics. We report a variety of active heterotrophic carbon processing mechanisms, including degradation of complex carbohydrate compounds by SAR406, SAR202, ACD39, and PAUC34f Together, these data help constrain the metabolic contributions from uncultivated groups in the nGOM during periods of low DO and suggest roles for these organisms in the breakdown of complex organic matter. Much of our current knowledge regarding microbial contributions to regions of low DO comes from numerous studies investigating naturally occurring, deep-water oxygen minimum zones (OMZs), such as those in the Eastern Tropical North and South Pacific, the Saanich Inlet, and the Arabian, Baltic, and Black Seas [4,5,6,7,8,9,10,11] In many of these systems, continual nutrient supply generates permanent or semipermanent decreases in oxygen, sometimes to the point of complete anoxia [4]. While parts of the nGOM hypoxic zone can become anoxic [1, 17], many areas maintain low oxygen concentrations even during peak hypoxia while the upper water column remains oxygenated [18,19,20]

Methods

Results

Conclusion