Mineral iron dissolution in Trichodesmium colonies: The role of O₂ and pH microenvironments

Abstract

Colonies of the N2‐fixing cyanobacterium Trichodesmium can harbor distinct chemical microenvironments that may assist the colonies in acquiring mineral iron from dust. Here, we characterized O2 and pH gradients in and around Trichodesmium colonies by microsensor measurements on > 170 colonies collected in the Gulf of Eilat over ∼ 2 months. O2 concentrations and pH values in the center of single colonies decreased in the dark due to respiration, reaching minimum values of 70 μmol L−1 and 7.7, whereas in the light, O2 and pH increased due to photosynthesis, reaching maximum values of 410 μmol L−1 and 8.6. Addition of dust and bacteria and increasing colony size influenced O2 and pH levels in the colonies, yet values remained within the range observed in single natural colonies. However, lower values down to 60 μmol L−1 O2 and pH 7.5 were recorded in the dark in dense surface accumulations of Trichodesmium. Using radiolabelled ferrihydrite, we examined the effect of these conditions on mineral iron dissolution and availability to Trichodesmium. Dark‐incubated colonies did not acquire iron from ferrihydrite faster than light‐incubated colonies, indicating that the dark‐induced decrease in pH and O2 within single colonies is too small to significantly increase mineral iron bioavailability. Yet, ligand‐promoted dissolution of ferrihydrite, a mechanism likely applied by Trichodesmum for acquiring mineral iron, did increase at the lower pH levels observed in surface accumulations. Thus, Trichodesmium surface blooms in their final stage may harbor chemical conditions that enhance the dissolution and bioavailability of mineral iron to the associated microbial community.

Unravelling Metal Speciation in the Microenvironment Surrounding Phytoplankton Cells to Improve Predictions of Metal Bioavailability

“… 12 − 15 Similarly, with natural Phaeocystis colonies, it was shown that Mn accumulation in the algae was significantly influenced by the pH and O 2 concentrations in the mucilaginous matrix in which the cells were imbedded. 16 In contrast, Eichner et al 17 reported that the utilization of Fe minerals by Trichodesmium colonies was little influenced by changes in pH and O 2 in and around the colonies. Moreover, two modeling studies showed that speciation of Si 18 and Cd 19 in the phycosphere differed from that in the bulk media.…”

Cyanobacterial blooms in oligotrophic lakes: Shifting the high‐nutrient paradigm

“…Eichner et al. (2020) showed plausible molecular evidence that colonies of Trichodesmium (marine cyanobacterium) can mediate Fe leaching. Fe leaching is a fundamental bacterial process for decoupling from Fe (Smolders et al., 2006), and may provide cyanobacteria with an increased benefit when competing with eukaryotes in oligotrophic systems.…”

“…4 bound in the sediment by modification of the redox potential, cyanobacteria can also mediate this process under oxic conditions via siderophore production and scavenging of bound Fe (Wilhelm & Trick, 1994), alleviating Fe limitation. Eichner et al (2020) showed plausible molecular evidence that colonies of Trichodesmium (marine cyanobacterium) can mediate Fe leaching. Fe leaching is a fundamental bacterial process for decoupling PO 3 − 4 from Fe (Smolders et al, 2006), and may provide cyanobacteria with an increased benefit when competing with eukaryotes in oligotrophic systems.…”

Quantitative models of nitrogen-fixing organisms

“…However, it has been challenged by recent studies that observe higher O 2 in a colony than the environment [232] and higher N 2 fixation rates in a free-floating filament than in a colony [84] . Despite that, there are still cases with lower O 2 in a colony during the middle of the day [84] , [233] and models would be useful in exploring the low O 2 effect as well as why free-floating filaments have higher rates of N 2 fixation.…”