Hydrogen Dynamics in Trichodesmium Colonies and Their Potential Role in Mineral Iron Acquisition

Abstract

N 2 -fixing cyanobacteria mediate H 2 fluxes through the opposing processes of H 2 evolution, which is a by-product of the N 2 fixation reaction, and H 2 uptake, which is driven by uptake hydrogenases. Here, we used microelectrodes to characterize H 2 and O 2 dynamics in single natural colonies of the globally important N 2 fixer Trichodesmium collected from the Gulf of Eilat. We observed gradually changing H 2 dynamics over the course of the day, including both net H 2 evolution and net H 2 uptake, as well as large differences in H 2 fluxes between individual colonies. Net H 2 uptake was observed in colonies amended with H 2 in both light and dark. Net H 2 evolution was recorded in the light only, reflecting light-dependent N 2 fixation coupled to H 2 evolution. Both net H 2 evolution and H 2 uptake rates were higher before 2 pm than later in the day. These pronounced H 2 dynamics in the morning coincided with strong net O 2 uptake and the previously reported diel peak in N 2 fixation. Later in the afternoon, when photosynthesis rates determined by O 2 measurements were highest, and N 2 fixation rates decrease according to previous studies, the H 2 dynamics were also less pronounced. Thus, the observed diel variations in H 2 dynamics reflect diel changes in the rates of O 2 consumption and N 2 fixation. Remarkably, the presence of H 2 strongly stimulated the uptake of mineral iron by natural colonies. The magnitude of this effect was dependent on the time of day, with the strongest response in incubations that started before 2 pm, i.e., the period that covered the time of highest uptake hydrogenase activity. Based on these findings, we propose that by providing an electron source for mineral iron reduction in N 2 -fixing cells, H 2 may contribute to iron uptake in Trichodesmium colonies.

A widely distributed hydrogenase oxidises atmospheric H2during bacterial growth

“…Some six phyla have now been described that are capable of atmospheric H 2 oxidation and, given the group 2a [NiFe]-hydrogenase is encoded by at least eight other phyla, others will likely soon be described. It is possible that atmospheric H 2 oxidation extends to other important groups, such as nitrite-oxidising Nitrospirota [31], methane-oxidising Proteobacteria [54], and potentially even oxygenic phototrophs; while Cyanobacteria are known to recycle endogenously-produced H 2 [27, 62, 63], it should be tested whether they can also scavenge exogenous H 2 . Indeed, while atmospheric H 2 oxidisers were only recently discovered [10, 14, 64], it is now plausible that these bacteria may represent the rule rather than the exception among aerobic H 2 oxidisers.…”

Ultrastructural Analysis of Cells From Bell Pepper (Capsicum annuum) Infected With Bell Pepper Endornavirus

“…Paramural bodies and membrane alterations have also been reported in cells infected with potato spindle tuber viroid (Hari, 1980). Plant viruses have been shown to target photosynthesis and negatively affect the chloroplast function, including host chlorophyll content (Zhao et al, 2016). Morphological changes of the chloroplast have been reported to be associated with plant virus or viroid infections (Hari, 1980;Lin and Langenberg, 1984).…”

Iron Uptake Mechanisms in Marine Phytoplankton

“…This implies that iron must be reduced before uptake, as in the eukaryotic yeast and Chlamydomonas models. It has been suggested that this reductive iron uptake strategy operates in many cyanobacteria (Kranzler et al, 2011(Kranzler et al, , 2013(Kranzler et al, , 2014Lis et al, 2015a;Rudolf et al, 2015;Xu et al, 2016;Eichner et al, 2019). The outer membrane has no obvious redox activity.…”

“…The ability of a cyanobacterium to solubilize ferrihydrite particles has been shown in Synechocystis PCC 6803 (Kranzler et al, 2016). The main mechanisms for dissolving mineral iron from dust include reductive dissolution and siderophore-mediated dissolution, both being thought to be involved in Trichodesmium dust utilization (Basu et al, 2019;Eichner et al, 2019). The presence of H 2 strongly stimulates mineral iron uptake by natural colonies FIGURE 5 | Iron sources available to marine phytoplankton and employed uptake pathways.…”

“…of Trichodesmium, and it has been suggested that H 2 acts as a source of electrons for the reduction of mineral iron by the cells (Eichner et al, 2019). However, Trichodesmium colonies host many associated siderophore-producing bacteria (Basu et al, 2019).…”