Independent iron and light limitation in a low-light-adapted <i>Prochlorococcus</i> from the deep chlorophyll maximum

Hawco, Nicholas J.; Fu, Fei-Xue; Yang, Ning; Hutchins, David A.; John, Seth G.

doi:10.1038/s41396-020-00776-y

“…Assuming a C:N ratio of 6.6, the corresponding Fe:C ratio, 8 μmol:mol, is below these Prochlorococcus Fe:C thresholds, suggesting that NO 3 ‐dependent growth in the cyclonic eddy would lead to Fe limitation. In contrast, some eukaryotic phytoplankton can grow at low irradiance with an Fe:C ratio below 5 μmol:mol (Maldonado & Price, 1996; Marchetti et al., 2006; Strzepek et al., 2012), likely because eukaryotic cells are able to support larger chlorophyll antennae than Prochlorococcus , decreasing the required number of photosynthetic reaction centers at low light (Bibby et al., 2003; Hawco et al., 2021; Strzepek et al., 2019). Lower photosynthetic Fe requirements among eukaryote phytoplankton could therefore allow NO 3 − drawdown without Fe limitation.…”

Section: Resultsmentioning

confidence: 99%

“…Relatively high iron requirements for Prochlorococcus photosynthesis may make them less competitive when NO 3 − supply increases. Experiments under DCM conditions with a low-light adapted Prochlorococcus (MIT1214 strain, LL1 ecotype) have indicated that the onset of Fe limitation is associated with an Fe:C ratio of 30-40 μmol:mol (Hawco et al, 2021), which is similar to the HLI Prochlorococcus strain MED4 when grown under low light (∼45 μmol:mol; Cunningham & John, 2017;Shire & Kustka, 2015). In the center of the cyclonic eddy, removal of 100 pM dFe was associated with the uptake of 2 μM NO 3 − .…”

Section: Prochlorococcus Fe Limitation In the Cyclonic Eddy?mentioning

confidence: 99%

Iron Depletion in the Deep Chlorophyll Maximum: Mesoscale Eddies as Natural Iron Fertilization Experiments

Hawco

¹

,

Barone

²

,

Church

³

et al. 2021

Global Biogeochemical Cycles

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Approximately 30% of the ocean's surface is subject to phytoplankton iron (Fe) limitation, especially in the Equatorial Pacific and Southern Oceans where upwelling provides a large flux of nitrate (NO 3 − ) and other nutrients (Moore et al., 2001(Moore et al., , 2013. Elsewhere, stratification of the upper ocean leads to depletion of NO 3 − , ammonia, and other bioavailable forms of nitrogen. In stratified oligotrophic gyres, shallow mixed layers also act to concentrate Fe deposited at the ocean's surface by atmospheric sources (Boyle et al., 2005;Sedwick et al., 2005). The large flux of Fe relative to NO 3 − in these ecosystems results in nitrogen limitation of photosynthesis and selects for phytoplankton like the cyanobacterium Prochlorococcus (Ward et al., 2013;Wu et al., 2000), whose small size allows them to outcompete other phytoplankton for recycled nitrogen species found at nanomolar concentrations (Morel et al., 1991).However, the same stratification that leads to Fe-rich conditions in the surface ocean can also impede Fe supply to the subsurface. Shallow mixed layers ensure that Fe derived from dust deposition does not reach the entirety of the euphotic zone, which can extend below 100 m in subtropical gyres. Stratification also limits the supply of regenerated Fe from below the euphotic zone. Indeed, a common feature of dFe profiles within subtropical gyres is a concentration minimum between 75 and 150 m (Bruland et al., 1994;Fitzsimmons et al., 2015;Sedwick et al., 2005). This subsurface dFe minimum often coincides with the deep chlorophyll maximum (DCM), a unique habitat where low irradiance drives phytoplankton photo-acclimation, increasing chlorophyll per cell to improve photosynthetic light capture (Letelier et al., 2004). Theoretical arguments suggest the increases in chlorophyll per cell should be matched by an equivalent increase in the number of Fe-bearing photosynthetic reaction

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“…Phytoplankton Fe-limitation at the DCM may emerge due to the upregulation of the Fe-rich photosynthetic apparatus under low light [59], which may increase Fe demand relative to supply [60] and thus low-light Prochlorococcus clades likely require more Fe than high-light clades [23]. Indeed, Prochlorococcus has relatively high photosynthetic Fe requirements under low irradiance, and there is evidence that LLI Prochlorococcus, in particular, is uniquely adapted to the low-Fe and low-light conditions typical of the DCM [23]. In some cases, the high Fe requirements of LLI Prochlorococcus may make them more sensitive to fluctuations in Fe concentration than eukaryotic phytoplankton [61].…”

Section: Resultsmentioning

confidence: 99%

“…Furthermore Fe-limitation or Fe/light co-limitation is a persistent feature of this layer [22]. Phytoplankton Fe-limitation at the DCM may emerge due to the upregulation of the Fe-rich photosynthetic apparatus under low light [59], which may increase Fe demand relative to supply [60] and thus low-light Prochlorococcus clades likely require more Fe than high-light clades [23]. Indeed, Prochlorococcus has relatively high photosynthetic Fe requirements under low irradiance, and there is evidence that LLI Prochlorococcus, in particular, is uniquely adapted to the low-Fe and low-light conditions typical of the DCM [23].…”

Section: Resultsmentioning

confidence: 99%

“…However, extent of siderophore uptake potential in cells belonging to LL-adapted clades which are uniquely adapted to waters deep in the euphotic zone is unknown. This is important because interactions between Fe and light limitation or Fe-light co-limitation may increase Fe demand for Prochlorococcus clades inhabiting deeper waters and the deep chlorophyll maximum layer (DCM) [22,23]. Also of interest is understanding what environmental features, in addition to Fe, are associated with Prochlorococcus siderophore uptake.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Hogle

¹

,

Hackl

²

,

Bundy

³

et al. 2021

Preprint

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Prochlorococcus is one of the most abundant photosynthesizing organisms in the oligotrophic oceans. Gene content variation among Prochlorococcus 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 low-light adapted Prochlorococcus populations from iron-depleted regions of the oligotrophic Pacific and S. Atlantic oceans: Prochlorococcus siderophore consumers were absent in the N. Atlantic ocean (higher iron flux) but constituted up to half of all Prochlorococcus genomes from metagenomes in the N. Pacific (lower iron flux). Prochlorococcus 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, particularly 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 Prochlorococcus.

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Iron depletion in the deep chlorophyll maximum: mesoscale eddies as natural iron fertilization experiments

Hawco

¹

,

Barone

²

,

Church

³

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Approximately 30% of the ocean's surface is subject to phytoplankton iron (Fe) limitation, especially in the Equatorial Pacific and Southern Oceans where upwelling provides a large flux of nitrate (NO 3 − ) and other nutrients (Moore et al., 2001(Moore et al., , 2013. Elsewhere, stratification of the upper ocean leads to depletion of NO 3 − , ammonia, and other bioavailable forms of nitrogen. In stratified oligotrophic gyres, shallow mixed layers also act to concentrate Fe deposited at the ocean's surface by atmospheric sources (Boyle et al., 2005;Sedwick et al., 2005). The large flux of Fe relative to NO 3 − in these ecosystems results in nitrogen limitation of photosynthesis and selects for phytoplankton like the cyanobacterium Prochlorococcus (Ward et al., 2013;Wu et al., 2000), whose small size allows them to outcompete other phytoplankton for recycled nitrogen species found at nanomolar concentrations (Morel et al., 1991).However, the same stratification that leads to Fe-rich conditions in the surface ocean can also impede Fe supply to the subsurface. Shallow mixed layers ensure that Fe derived from dust deposition does not reach the entirety of the euphotic zone, which can extend below 100 m in subtropical gyres. Stratification also limits the supply of regenerated Fe from below the euphotic zone. Indeed, a common feature of dFe profiles within subtropical gyres is a concentration minimum between 75 and 150 m (Bruland et al., 1994;Fitzsimmons et al., 2015;Sedwick et al., 2005). This subsurface dFe minimum often coincides with the deep chlorophyll maximum (DCM), a unique habitat where low irradiance drives phytoplankton photo-acclimation, increasing chlorophyll per cell to improve photosynthetic light capture (Letelier et al., 2004). Theoretical arguments suggest the increases in chlorophyll per cell should be matched by an equivalent increase in the number of Fe-bearing photosynthetic reaction

show abstract

Independent iron and light limitation in a low-light-adapted Prochlorococcus from the deep chlorophyll maximum

Cited by 18 publications

References 20 publications

Iron Depletion in the Deep Chlorophyll Maximum: Mesoscale Eddies as Natural Iron Fertilization Experiments

Iron Depletion in the Deep Chlorophyll Maximum: Mesoscale Eddies as Natural Iron Fertilization Experiments

Siderophores as an iron source for Prochlorococcus in deep chlorophyll maximum layers of the oligotrophic ocean

Iron depletion in the deep chlorophyll maximum: mesoscale eddies as natural iron fertilization experiments

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