Regulation of the Phytoplankton Heme b Iron Pool During the North Atlantic Spring Bloom

Abstract

Heme b is an iron-containing co-factor in hemoproteins. Heme b concentrations are low (<1 pmol L -1 ) in iron limited phytoplankton in cultures and in the field. Here, we determined heme b in marine particulate material (>0.7 μm) from the North Atlantic Ocean (GEOVIDE cruise – GEOTRACES section GA01), which spanned several biogeochemical regimes. We examined the relationship between heme b abundance and the microbial community composition, and its utility for mapping iron limited phytoplankton. Heme b concentrations ranged from 0.16 to 5.1 pmol L -1 (median = 2.0 pmol L -1 , n = 62) in the surface mixed layer (SML) along the cruise track, driven mainly by variability in biomass. However, in the Irminger Basin, the lowest heme b levels (SML: median = 0.53 pmol L -1 , n = 12) were observed, whilst the biomass was highest (particulate organic carbon, median = 14.2 μmol L -1 , n = 25; chlorophyll a : median = 2.0 nmol L -1 , n = 23) pointing to regulatory mechanisms of the heme b pool for growth conservation. Dissolved iron (DFe) was not depleted (SML: median = 0.38 nmol L -1 , n = 11) in the Irminger Basin, but large diatoms ( Rhizosolenia sp.) dominated. Hence, heme b depletion and regulation is likely to occur during bloom progression when phytoplankton class-dependent absolute iron requirements exceed the available ambient concentration of DFe. Furthermore, high heme b concentrations found in the Iceland Basin and Labrador Sea (median = 3.4 pmol L -1 , n = 20), despite having similar DFe concentrations to the Irminger Basin, were attributed to an earlier growth phase of the extant phytoplankton populations. Thus, heme b provides a snapshot of the cellular activity in situ and could both be used as indicator of iron limitation and contribute to understanding phytoplankton adaptation mechanisms to changing iron supplies.

Heme b distributions through the Atlantic Ocean: evidence for “anemic” phytoplankton populations

“…Our observations are confirmed by bioassay experiments that showed the eastern boundary of the Subtropical South Atlantic Gyre was nitrate-iron co-limited during the period of the cruise 45 . The good agreement between the heme b measurements and the bioassay experiments of Browning, et al 45 reinforces previous comparisons with other approaches for mapping iron-limited phytoplankton communities 36 that included the dissolved iron:nitrate ratio 56 , modified Si * tracer [57][58][59] and satellite-derived quantum yield of fluorescence Φ sat 60,61 . Heme b measurements thus appeared to successfully map iron limited phytoplankton by depicting the momentary condition of the phytoplankton cells in situ.…”

“…In laboratory studies, values of heme b:POC below 0.10 μmol mol −1 were indicative of iron-limited phytoplankton 15,16 , and similar values have been determined for field phytoplankton communities in the iron -limited post-bloom Iceland Basin 35 and low-iron Southern Ocean 16,35 . In case of Irminger Basin, Louropoulou et al 36 www.nature.com/scientificreports www.nature.com/scientificreports/ high iron concentrations (≥0.30 nmol L −1 ), indicating iron limitation resulting from the high iron requirements of the extant phytoplankton population.…”

“…S1) suggest that both the spatial and the vertical distribution of heme b concentrations in the Atlantic Ocean were strongly influenced by biomass, as observed previously 15 . However, heme b was shown in previous studies to vary due to phytoplankton regulation strategies that occur as adaptation responses to iron-limitation 16,36 , thus weakening the overall correlation of heme b relative to POC.…”

“…4) followed by the Coastal Tropical North Atlantic (median = 4.2 nmol L −1 , n = 14) ( Table 2). In addition, heme b was also enhanced in the highly productive subpolar areas (Iceland Basin, Greenland Shelf and Labrador Sea) which were sampled during the spring bloom in 2014 (range 0.16-4.6 pmol L −1 , median = 2.2 pmol L −1 , n = 48) 36 . However, the Irminger Basin deviated from this Heme b correlated with both POC (Spearman's rho, r = 0.41, n = 465, p < 0.01) and chl a (Spearman's rho, r = 0.56, n = 490, p < 0.01) ( Supplementary Fig.…”

“…In order to examine the changes of heme b relative to biomass as indicated by POC and chl a, we calculated the ratios of heme b:POC and heme b: chl a 16,35 . The heme b:POC ratio represents the heme b per unit carbon derived from the total particulate organic matter and previous field studies showed that this ratio varied as a result of iron availability 15,16,35,36 . The ratio heme b: chl a corresponds to organic matter originating from phytoplankton, but because of intracellular chlorophyll variability, can also be influenced by light-and nutrient-driven changes in the photosystem.…”