Heme b in marine phytoplankton and particulate material from the North Atlantic Ocean

Honey, David J.; Gledhill, Martha; Bibby, Thomas S.; Legiret, François-Eric; Pratt, Nicola; Hickman, Anna E.; Lawson, Tracy; Achterberg, Eric P.

doi:10.3354/meps10367

Cited by 27 publications

(83 citation statements)

References 65 publications

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“…Maximum average heme b : chl a and heme b : TPC ratios were observed several days before the chl a maximum at a time corresponding to the initiation of the primary phytoplankton bloom. The heme b : chl a and heme b : TPC ratio was also considerably higher than that observed in phytoplankton monocultures, which have previously been reported only for the end of the exponential phase [6, 13]. As the period of maximum heme b : chl a and heme b : TPC ratios was pre-bloom, it is likely that the relative increase in heme b is associated with elevated concentrations of heme b within the photosynthetic phytoplankton population, rather than relative changes in the abundance of heterotrophs and phototrophs or shifts in community composition.…”

Section: Discussionmentioning

confidence: 57%

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Abundance of the iron containing biomolecule, heme b, during the progression of a spring phytoplankton bloom in a mesocosm experiment

et al. 2017

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Concentrations of heme b were determined in a mesocosm experiment situated in Gullmar Fjord off Sweden. The mesocosm experiment lasted for ca. one hundred days and was characterised by the growth of a primary nutrient replete and a secondary nutrient deplete phytoplankton bloom. Heme b varied between 40 ± 10 pmol L-1 in the prebloom period up to a maximum of 700 ± 400 pmol L-1 just prior to the time of the primary chlorophyll a maximum. Thereafter, heme b concentrations decreased again to an average of 120 ± 60 pmol L-1. When normalised to total particulate carbon, heme b was most abundant during the initiation of the nutrient replete spring bloom, when ratios reached 52 ± 24 μmol mol-1; ten times higher than values observed both pre and post the primary bloom. Concentrations of heme b correlated with those of chlorophyll a. Nevertheless, differences were observed in the relative concentrations of the two parameters, with heme b concentrations increasing relative to chlorophyll a during the growth of the primary bloom, decreasing over the period of the secondary bloom and increasing again through the latter period of the experiment. Heme b abundance was therefore influenced by nutrient concentrations and also likely by changing community composition. In half of the mesocosms, pCO2 was elevated and maintained at ca.1000 μatm, however we observed no significant differences between heme b in plus or ambient pCO2 mesocosms, either in absolute terms, or relative to total particulate carbon and chlorophyll a. The results obtained in this study contribute to our understanding of the distribution of this significant component of the biogenic iron pool, and provide an iron replete coastal water end member that aids the interpretation of the distributions of heme b in more iron deplete open ocean waters.

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Section: Discussionmentioning

confidence: 57%

“…However, the application of identical methods as previously used to determine chl a : heme b relationships in open ocean systems [6, 12], permits a comparison to the coastal fjord of this study.…”

Section: Methodsmentioning

confidence: 99%

Abundance of the iron containing biomolecule, heme b, during the progression of a spring phytoplankton bloom in a mesocosm experiment

et al. 2017

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“…More recently, heme in marine particulate organic matter has been directly measured at picomolar concentrations (19, 20). Few studies have examined turnover rates of algal iron in the marine environment, but if we assume an average contribution of 35 pM diatom-derived particulate organic iron during natural iron-fertilized diatom blooms (13, 43) and a mobilization rate of 5% to 17% particulate algal iron day −1 into heterotrophic bacteria biomass (45) and that 40% of diatom iron is in the form of heme (28), this would translate to a maximum rate of between 0.7 and 2.4 pmol diatom heme liter −1 ·day −1 transferred into heterotrophic bacteria during bloom remineralization.…”

Section: Discussionmentioning

confidence: 99%

“…Heme is an iron-containing heterocyclic enzyme cofactor, is biologically ubiquitous, and is widespread in the marine environment (18). Prior work has shown that heme comprises approximately 20% of the total iron pool in marine phytoplankton cultures and is present in similar proportions in marine particulate organic matter (19, 20). Because of its prevalence in marine phytoplankton, heme may be a potentially abundant local iron source for bacteria living in close proximity to phytoplankton.…”

Section: Introductionmentioning

confidence: 99%

Direct Heme Uptake by Phytoplankton-Associated Roseobacter Bacteria

2017

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Ecosystem productivity in large regions of the surface ocean is fueled by iron that has been microbially regenerated from biomass. Currently, the specific microbes and molecules that mediate the transfer of recycled iron between microbial trophic levels remain largely unknown. We characterized a marine bacterial heme transporter and verified its role in acquiring heme, an abundant iron-containing enzyme cofactor. We present evidence that after host cell lysis, phytoplankton-associated bacteria directly extract heme and hemoproteins from algal cellular debris in order to fulfill their iron requirements and that the regulation of this process may be modulated by host cues. Direct heme transport, in contrast to multistep extracellular processing of hemoproteins, may allow certain phytoplankton-associated bacteria to rapidly extract iron from decaying phytoplankton, thus efficiently recycling cellular iron into the wider microbial loop.

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“…In the marine environment, heme has been detected at picomolar concentrations in particulate material (13) and at nanomolar concentrations in the dissolved phase in estuaries (14). Heme is also susceptible to photochemical degradation in the surface ocean; thus, heme accumulation is presumably be limited to low-light environments.…”

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confidence: 99%

Utilization of Heme as an Iron Source by Marine Alphaproteobacteria in the Roseobacter Clade

Roe

Hogle

Barbeau

2013

Appl Environ Microbiol

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The bioavailability and utilization of porphyrin-bound iron, specifically heme, by marine microorganisms have rarely been examined. This study used Ruegeria sp. strain TrichCH4B as a model organism to study heme acquisition by a member of the Roseobacter clade. Analogs of known heme transporter proteins were found within the Ruegeria sp. TrichCH4B genome. The identified heme uptake and utilization system appears to be functional, as the heme genes were upregulated under iron stress, the bacterium could grow on ferricporphyrin complexes as the sole iron source, and internalization of 55 Fe from ferric protoporphyrin IX was observed. The potential ability to utilize heme in the Roseobacter clade appears to be common, as half of the isolates in the RoseoBase database were found to have a complete heme uptake system. A degenerate primer set was designed and successfully used to identify the putative heme oxygenase gene (hmus) in the roseobacter heme uptake system from diverse nonenriched marine environments. This study found that members of the Roseobacter clade are capable of utilizing heme as an iron source and that this capability may be present in all types of marine environments. The results of this study add a new perspective to the current picture of iron cycling in marine systems, whereby relatively refractory intracellular pools of heme-bound iron may be taken up quickly and directly reincorporated into living bacteria without previous degradation or the necessity of a siderophore intermediate.

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Heme b in marine phytoplankton and particulate material from the North Atlantic Ocean

Cited by 27 publications

References 65 publications

Abundance of the iron containing biomolecule, heme b, during the progression of a spring phytoplankton bloom in a mesocosm experiment

Abundance of the iron containing biomolecule, heme b, during the progression of a spring phytoplankton bloom in a mesocosm experiment

Direct Heme Uptake by Phytoplankton-Associated Roseobacter Bacteria

Utilization of Heme as an Iron Source by Marine Alphaproteobacteria in the Roseobacter Clade

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