Response of heterotrophic bacteria in a mesoscale iron enrichment in the northeast subarctic Pacific Ocean (original) (raw)
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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.
Aquatic Microbial Ecology, 2007
It is now established that iron (Fe) availability controls phytoplankton productivity and community structure in ca. 50% of the Pacific Ocean's surface waters and that heterotrophic bacterioplankton may also be either directly or indirectly Fe-limited. Proxy indicators of Fe-stress are available for the phototrophic community (e.g. ferredoxin/flavodoxin ratios) but are lacking for the heterotrophic bacterioplankton. While current analytical tools provide valuable information with regard to micronutrient chemistry and speciation, they do not provide insight into the relative bioavailability of different Fe sources. We present the results of a field trial in an oceanic system of a tool that allows for the assessment of Fe bioavailability in natural systems: the Fe-responsive bioluminescent heterotrophic bacterial reporter. Fe bioavailability was monitored with this tool at the scale of the Eastern Pacific Basin during the mature phase of the El Niño event of 2002. The results demonstrate significant spatial variance, highlighted by regions of decreased Fe availability at equatorial stations along the transect. Using this tool in combination with radiotracer studies of bacterial growth and community Fe uptake, we provide insight into system Fe chemistry and the status of the heterotrophic bacterial community. Our results indicate that different environments with similar concentrations of total Fe can demonstrate different Fe bioavailabilities. Moreover, the small particulate size fraction (0.2 to 0.8 µm) appears to buffer artificially induced variations in Fe bioavailability, implying that studies of Fe bioavailability need to be extended beyond those in the dissolved (< 0.2 µm) size class.
Marine bacteria and biogeochemical cycling of iron in the oceans
Fems Microbiology Ecology, 1999
Prokaryotic microbes play a critical role in oceanic Fe cycling. They contain most of the biogenic Fe in offshore waters and are responsible for a large portion of the Fe uptake by the plankton community. In the subarctic North Pacific, surface populations of heterotrophic species assimilate more than 50% of the dissolved Fe and thus compete directly with phytoplankton for this limiting resource. In oligotrophic tropical and subtropical waters, photosynthetic bacteria become more important in Fe cycling as the number of unicellular cyanobacteria increases and the nitrogen-fixing Trichodesmium, which contains most of the biogenic Fe in the mixed layer, becomes abundant. Like their terrestrial counterparts, heterotrophic and phototrophic marine bacteria produce Fe-binding siderophores that are involved in Fe acquisition. Evidence exists that bacteria may modify Fe chemistry in the sea through the production of these ligands and thereby play a significant role in regulating production of eukaryotic phytoplankton. z
The importance of siderophores in iron nutrition of heterotrophic marine bacteria
Limnology and Oceanography, 1999
Recent studies demonstrate that dissolved iron in seawater is bound to strong organic complexes that have stability constants comparable to those of microbial iron chelates. We examined iron acquisition by seven strains of heterotrophic marine bacteria from a number of siderophore-iron complexes, including desferrioxamine B (DFB) and marine siderophores partially purified from iron-limited cultures. Hydroxamate siderophores were detected in the supernatants of four strains, one of which also produced a catechol. All strains transported iron bound to siderophores regardless of whether or not they produced their own, and the majority took up iron bound to DFB. Uptake rates of Fe siderophores were similar among iron-limited strains and among ligands. Transport of FeDFB by strain Neptune was enhanced 20 times by iron limitation, whereas uptake of unchelated iron (FeЈ) did not saturate at the highest concentration tested and was not regulated by the iron nutritional status of the cells. The half-saturation constant for uptake of FeDFB by Neptune was 15 nM, the lowest reported for an Fe siderophore in any microorganism. Iron uptake by the catechol-producing strain, LMG1, differed markedly in two respects from the other strains: LMG1 could not take up iron bound to DFB; furthermore, transport of FeЈ by iron-limited LMG1 was 10 times faster than the other strains and was upregulated 46 times compared to Fe-sufficient cells. Experimental evidence suggests that iron transport by LMG1 may be mediated by surface-associated catechol siderophores that scavenge inorganic ferric species as well as iron bound to weaker complexes, such as EDTA (ethylenediaminetetraacetic acid). The combined results of the study highlight the importance of siderophores in iron transport by heterotrophic marine bacteria and suggest, by inference, that bacteria may rely on siderophores to acquire iron in situ.
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.
Progress in Oceanography, 2005
To verify the hypothesis that the growth of phytoplankton in the Western Subarctic Gyre (WSG), which is located in the northwest subarctic PaciWc, is suppressed by low iron (Fe) availability, an in situ Fe fertilization experiment was carried out in the summer of 2001. Changes over time in the abundance and community structure of phytoplankton were examined inside and outside an Fe patch using phytoplankton pigment markers analyzed by high-performance liquid chromatography (HPLC) and Xow cytometry (FCM). In addition, the abundance of heterotrophic bacteria was also investigated by FCM. The chlorophyll a concentration was initially ca. 0.9 g l ¡1 in the surface mixed layer where diatoms and chlorophyll b-containing green algae (prasinophytes and chlorophytes) were predominant in the chlorophyll biomass. After the iron enrichment, the chlorophyll a concentration increased up to 9.1 g l ¡1 in the upper 10 m inside the Fe patch on Day 13. At the same time, the concentration of fucoxanthin (a diatom marker) increased 45-fold in the Fe patch, and diatoms accounted for a maximum 69% of the chlorophyll biomass. This result was consistent with a microscopic observation showing that the diatom Chaetoceros debilis had bloomed inside the Fe patch. However, chlorophyllide a concentrations also increased in the Fe patch with time, and reached a maximum of 2.2 g l ¡1 at 5 m depth on Day 13, suggesting that a marked abundance of senescent algal cells existed at the end of the experiment. The concentration of peridinin (a dinoXagellate marker) also reached a maximum 24-fold, and dinoXagellates had contributed signiWcantly (>15%) to the chlorophyll biomass inside the Fe patch by the end of the experiment. Concentrations (K. Suzuki).
Frontiers in Marine Science, 2018
Organic ligands play a key role controlling trace metal bioavailability in the world's oceans, yet the species-specific requirements determining whether certain iron forms can be metabolized largely remain unclear. Siderophores are considered relevant within the pool of ligands keeping iron soluble. We used desferrioxamine B (DFB) to study the siderophore's effect on cultures of Skeletonema costatum and Alexandrium catenella. The experimental approach used semi-continuous additions of iron(II) and DFB over time, reaching final concentrations of 1 and 10 nM Fe and 10-10,000 nM DFB. The negative effect of DFB on growth in S. costatum was evident and sharp until day 9 for treatments above 500 nM. Delayed growth occurred at 10,000 nM, reaching ∼80% of cell density in Controls under both iron conditions. Alexandrium catenella exhibited a less severe negative effect of DFB on growth, only significant at 10,000 nM, while growth was enhanced at lowest DFB. Total bacterial abundance in diatom and dinoflagellate cultures presented inverse trends. While negatively correlated to DFB in diatom cultures, bacteria showed highest abundances in high DFB treatments in dinoflagellate cultures. Delayed growth exhibited in S. costatum at the highest DFB, indicates that favorable changes for Fe uptake occurred over time, suggesting the involvement of other mechanisms facilitating the diatom cell membrane reduction. Overall, unaffected growth in A. catenella suggests that this species can use FeDFB and therefore has the capacity to access strongly complexed Fe sources. Contrasting responses in the bacterial community associated with each species highlight the complexity of these interactions, while suggesting that for A. catenella it may represent an advantage for acquiring Fe. These results demonstrated the capacity for different uptake strategies among phytoplankton species of different functional groups and underlines the necessity to broaden the study of iron bioavailability on a species basis, alongside interaction with other microbial components such bacteria, to reflect interactions in natural ecosystems.