scholarly journals Metabolic roles of uncultivated bacterioplankton lineages in the northern Gulf of Mexico “Dead Zone”

2016 ◽  
Author(s):  
J. Cameron Thrash ◽  
Kiley W. Seitz ◽  
Brett J. Baker ◽  
Ben Temperton ◽  
Lauren E. Gillies ◽  
...  

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 those belonging to 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.ImportanceDead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon—many of which occur in bacterioplankton from poorly understood lineages—have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these “microbial dark matter” taxa during hypoxia.

mBio ◽  
2017 ◽  
Vol 8 (5) ◽  
Author(s):  
J. Cameron Thrash ◽  
Kiley W. Seitz ◽  
Brett J. Baker ◽  
Ben Temperton ◽  
Lauren E. Gillies ◽  
...  

ABSTRACT 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. 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. IMPORTANCE Dead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon—many of which occur in bacterioplankton from poorly understood lineages—have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these “microbial dark matter” taxa during hypoxia. IMPORTANCE Dead zones receive their name primarily from the reduction of eukaryotic macrobiota (demersal fish, shrimp, etc.) that are also key coastal fisheries. Excess nutrients contributed from anthropogenic activity such as fertilizer runoff result in algal blooms and therefore ample new carbon for aerobic microbial metabolism. Combined with strong stratification, microbial respiration reduces oxygen in shelf bottom waters to levels unfit for many animals (termed hypoxia). The nGOM shelf remains one of the largest eutrophication-driven hypoxic zones in the world, yet despite its potential as a model study system, the microbial metabolisms underlying and resulting from this phenomenon—many of which occur in bacterioplankton from poorly understood lineages—have received only preliminary study. Our work details the metabolic potential and gene expression activity for uncultivated lineages across several low DO sites in the nGOM, improving our understanding of the active biogeochemical cycling mediated by these “microbial dark matter” taxa during hypoxia.


Dead Zones ◽  
2021 ◽  
pp. 52-71
Author(s):  
David L. Kirchman

This chapter discusses what happened around 1950 that led to the expansion of dead zones. For the Gulf of Mexico, there are many reasons to think the flow of the Mississippi River has changed since the days of Mark Twain, considering the construction of so many levees, dikes, floodways, spillways, weirs, and revetments. Rain-absorbing grasslands and forests have been replaced by asphalt, roof shingles, and other hydrophobic material that hasten rainwater to the Gulf. But the flow of the Mississippi has not changed enough to explain why the Gulf dead zone grew around 1950. As the chapter discusses, what did change was nutrients. It shows that concentrations doubled in the Mississippi River from the 1930s to the 1990s, which stimulated algal growth and production of organic material that eventually led to depletion of dissolved oxygen. In addition to creating dead zones, the increase in nutrients has stimulated harmful algal blooms, leading to fish kills and beach closings.


Dead Zones ◽  
2021 ◽  
pp. 72-88
Author(s):  
David L. Kirchman

When it became clear that nutrients cause the rise of dead zones, scientists next examined the possible sources of the nutrients. This chapter argues the biggest source today is agriculture. The expansion of the Gulf of Mexico dead zone directly follows the huge increase in agricultural productivity, especially for corn. Yields increased over six times since 1930 in part because farmers used more fertilizer, “to give the land a kick.” As the chapter explains, Nancy Rabalais and Gene Turner found a direct link between fertilizer use and nutrient levels in the Mississippi River. In spite of opposition from agribusinesses, their work led to the formation of a White House committee and passage of legislation to support work on the hypoxia problem. Agriculture is also the main source of nutrients feeding dead zones in other regions of the world. The chapter later points out that the biggest user of fertilizer is now China, where excessive nutrients have caused massive harmful algal blooms and other environmental problems.


Dead Zones ◽  
2021 ◽  
pp. 21-35
Author(s):  
David L. Kirchman

This chapter describes the discovery of coastal dead zones, such as the Gulf of Mexico and Chesapeake Bay in North America and the Baltic and Black Seas in Europe. Gene Turner sailed out of Pascagoula, Mississippi, in the spring of 1975, on the first of seven cruises that led to the discovery of the Gulf of Mexico dead zone. In the Chesapeake Bay, an unlikely environmentalist, Charles Officer, sounded the alarm in 1984. The biggest dead zone, however, is the Baltic Sea. Even as early as 1969, ecologists feared hypoxia was turning the Baltic into a “biological desert.” The northwest shelf of the Black Sea turned hypoxic in the 1970s, which killed bottom-dwelling fish like goby and flounder. Many coastal regions around the world have low oxygen waters that devastate marine life and habitats. The early studies emphasized one or two of three ingredients—sewage, fresh water, and plant nutrients—thought to be essential in creating a dead zone. This chapter and Chapter 3 discuss these ingredients before revealing which is most important.


2018 ◽  
Vol 7 (9) ◽  
Author(s):  
J. Cameron Thrash ◽  
Brett J. Baker ◽  
Kiley W. Seitz ◽  
Ben Temperton ◽  
Lauren Gillies Campbell ◽  
...  

Coastal regions experiencing declining dissolved oxygen are increasing in number and severity around the world. However, despite the importance of microbial metabolism in coastal hypoxia, few metagenomic surveys exist.


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