Marine bacteria and biogeochemical cycling of iron in the oceans (original) (raw)
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Limnology and Oceanography, 2014
The response of heterotrophic bacteria in a mesoscale iron (Fe) enrichment was measured in the northeast subarctic Pacific Ocean in July 2002. Addition of FeSO 4 increased the dissolved Fe concentration in the fertilized patch to 2-3 nmol L 21 and triggered an increase in concentration of Fe(III)-binding ligands that complexed all of the dissolved Fe. Two to three days later, leucine incorporation rate and specific growth rate of bacteria doubled. Physiological markers of bacterial Fe nutritional state varied during the experiment as the microbial community assimilated the added Fe. Cellular uptake rate of an iron-siderophore complex, 55 Fe-ferrioxamine B (FB), increased twofold to fourfold over background values and then declined by day 4.5. The fastest rate of Fe-FB uptake on day 2.5 coincided roughly with a transient increase in outer-membrane, 55 Fe-FB-binding protein(s) in bacteria and with the peak in ligand concentration. Maximum potential uptake rate of inorganic Fe (V max) was 8 zmol Fe bacterium 21 h 21 prior to Fe enrichment and then decreased by a factor of four within 2.5 d of fertilizing the patch as bacteria became Fe sufficient. V max gradually increased by day 6.5 as the bacterial community re-entered iron deficiency. Similar changes in growth and Fe uptake kinetics were observed after a second Fe addition. Heterotrophic bacteria in the subarctic Pacific were Fe-deficient and responded directly to Fe addition by up-regulating pathways for Fe-siderophore acquisition and assimilating complexed Fe. The observation that increases in Fe uptake pathways and production were synchronous is consistent with the hypothesis that bacterial growth was directly limited by Fe.
Journal of Experimental Marine Biology and Ecology, 2007
While it has been shown that phytoplankton productivity and community structure are influenced by the availability of Fe in several high nutrient-low chlorophyll (HNLC) regions of the world's oceans, the influence of Fe on the bacterial community remains unresolved. Therefore, we sampled water from the Peruvian upwelling region of the equatorial Pacific Ocean and examined how bacterial community structure changes with Fe additions (1.5 nM, 0.5 nM above ambient) and sequestration, which was accomplished by additions of the fungal siderophore desferrioxamine B (DFB) (1.0 nM, 5.0 nM). We hypothesized that either 1) the bacterial communities are generally Fe-limited and thus show positive responses to Fe addition; or 2) that bacteria form the equivalent of response groups and show a limited number of responses to Fe addition; or else 3) that the bacterial communities show no response to Fe addition. Using Terminal Restriction Fragment Length Polymorphism analysis, we found that the eubacterial community changed in response to Fe. Whereas the overall community shows little abundance and richness responses to Fe availability, bacteria can be arranged into response groups showing divergent responses to Fe addition. With validated cluster analysis, we found that the bacterial community consisted of four response groups. One group showed strong positive responses to increasing Fe availability, while another group showed strong negative responses. The abundance patterns of the final two groups showed no response to alterations in Fe availability, although one persisted at a high abundances and the other a low abundance. These results reveal that it may be difficult to describe a singular bacterial community response to changes in Fe availability, and that understanding the influence of Fe on bacteria dynamics may require an understanding of the different responses of individual sub-groups of bacteria within the microbial community.
bioRxiv (Cold Spring Harbor Laboratory), 2021
Prochlorococcus and Synechococcus are the most abundant photosynthesizing organisms in the oceans. Gene content variation among picocyanobacterial populations in separate ocean basins often mirrors the selective pressures imposed by the region's distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in Synechococcus and low-light adapted Prochlorococcus populations from deep chlorophyll maximum layers of iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher new iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower new iron flux). Picocyanobacterial siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, especially at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of marine picocyanobacteria.
The ISME Journal, 2022
Prochlorococcus and Synechococcus are the most abundant photosynthesizing organisms in the oceans. Gene content variation among picocyanobacterial populations in separate ocean basins often mirrors the selective pressures imposed by the region's distinct biogeochemistry. By pairing genomic datasets with trace metal concentrations from across the global ocean, we show that the genomic capacity for siderophore-mediated iron uptake is widespread in Synechococcus and low-light adapted Prochlorococcus populations from deep chlorophyll maximum layers of iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher new iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower new iron flux). Picocyanobacterial siderophore consumers, like many other bacteria with this trait, also lack siderophore biosynthesis genes indicating that they scavenge exogenous siderophores from seawater. Statistical modeling suggests that the capacity for siderophore uptake is endemic to remote ocean regions where atmospheric iron fluxes are the smallest, especially at deep chlorophyll maximum and primary nitrite maximum layers. We argue that abundant siderophore consumers at these two common oceanographic features could be a symptom of wider community iron stress, consistent with prior hypotheses. Our results provide a clear example of iron as a selective force driving the evolution of marine picocyanobacteria.
Response of bacterioplankton to iron fertilization in the Southern Ocean
Limnology and Oceanography, 2004
We studied the bacterial response to Fe fertilization over 3 weeks during the second iron-enrichment experiment (EisenEx) in the Southern Ocean. Bacterial abundance in the Fe-fertilized patch increased over the first 12 d following Fe release and remained about twice as high as outside the Fe-fertilized patch until the end of the experiment. Bacterial production peaked a few days after each of the three Fe releases inside the Fe-fertilized patch, reaching rates two to three times higher than outside the patch. Besides the peaks in leucine and thymidine incorporation following Fe release, bacterial production was not significantly higher inside the patch than outside, suggesting direct limitation of bacterial growth by Fe. Bacterial aminopeptidase activity roughly followed the increase in bacterial abundance, whereas cell-specific ␣and -glucosidase were higher inside the Fe-fertilized patch. The diversity of -glucosidases was determined by capillary electrophoresis zymography. The different -glucosidases showed much higher activity levels inside the patch than in the surrounding waters, and three additional -glucosidases constituting ϳ55% of the total -glucosidase activity were present inside the Fe-fertilized patch from day 9 onward. No major changes in response to Fe fertilization were detected in the phylogenetic composition of the bacterioplankton community, as determined by 16S rDNA fingerprinting, indicating a remarkable adaptation of the bacterioplankton community to episodic iron inputs. This stability on the phylogenetic level is contrasted by the dramatic qualitative and quantitative changes in ectoenzymatic activity.
Frontiers in Earth Science, 2015
Evidence for Fe(II) oxidation and deposition of Fe(III)-bearing minerals from anoxic or redox-stratified Precambrian oceans has received support from decades of sedimentological and geochemical investigation of Banded Iron Formations (BIF). While the exact mechanisms of Fe(II) oxidation remains equivocal, reaction with O 2 in the marine water column, produced by cyanobacteria or early oxygenic phototrophs, was likely. In order to understand the role of cyanobacteria in the deposition of Fe(III) minerals to BIF, we must first know how planktonic marine cyanobacteria respond to ferruginous (anoxic and Fe(II)-rich) waters in terms of growth, Fe uptake and homeostasis, and Fe mineral formation. We therefore grew the common marine cyanobacterium Synechococcus PCC 7002 in closed bottles that began anoxic, and contained Fe(II) concentrations that span the range of possible concentrations in Precambrian seawater. These results, along with cell suspension experiments, indicate that Fe(II) is likely oxidized by this strain via chemical oxidation with oxygen produced during photosynthesis, and not via any direct enzymatic or photosynthetic pathway. Imaging of the cell-mineral aggregates with scanning electron microscopy (SEM) and confocal laser scanning microscopy (CLSM) are consistent with extracellular precipitation of Fe(III) (oxyhydr)oxide minerals, but that >10% of Fe(III) sorbs to cell surfaces rather than precipitating. Proteomic experiments support the role of reactive oxygen species (ROS) in Fe(II) toxicity to Synechococcus PCC 7002. The proteome expressed under low Fe conditions included multiple siderophore biosynthesis and siderophore and Fe transporter proteins, but most siderophores are not expressed during growth with Fe(II). These results provide a mechanistic and quantitative framework for evaluating the geochemical consequences of perhaps life's greatest metabolic innovation, i.e., the evolution and activity of oxygenic photosynthesis, in ferruginous Precambrian oceans.
Response of marine bacterial community composition to iron additions in three iron-limited regimes
Limnology and Oceanography, 2001
In high-nutrient low-chlorophyll (HNLC) regimes, iron additions consistently result in primary productivity increases, and the phytoplankton community shifts from small species toward large diatoms. Heterotrophic bacterial production and abundance also increase in HNLC Fe addition experiments, but whether changes in bacterioplankton community composition also occur when Fe is added is unknown. We used trace metal clean shipboard incubation experiments, and molecular biological methods to examine this question in three Fe-limited environments: the subarctic Pacific, the subantarctic Southern Ocean, and the California coastal upwelling region. After Fe additions and subsequent phytoplankton community shifts, changes in bacterial community composition were examined using denaturing gradient gel electrophoresis and terminal restriction fragment length polymorphism of polymerase chain reaction-amplified bacterial 16S rRNA genes. Responsive bacterial phylotypes in either ϩFe or control treatments were classified using phylogenetic analyses of DNA sequences. In general, iron-mediated changes in bacterial communities in all three environments were surprisingly minor compared to the changes in phytoplankton community composition. Responsive phylotypes were mostly ␥-proteobacteria in the subarctic and California HNLC areas, but no changes were noted in the subantarctic experiments. Although bacterial growth and biomass are closely linked to phytoplankton-derived carbon supplies, our results suggest that on the time scale of our experiments (4-5 d), species composition of algal and bacterial communities can be decoupled in Fe-limited waters.