Mineral iron utilization by natural and cultured Trichodesmium and associated bacteria

Abstract

The high iron (Fe) demands of Trichodesmium, a keystone nitrogen‐fixing cyanobacterium, are often met by dust deposition at the ocean surface. Following up on our findings of unique dust capturing and processing by Trichodesmium, we explored the ability of natural Trichodesmium colonies from the Gulf of Aqaba and Fe‐limited laboratory culture (IMS101) to obtain Fe from the mineral ferrihydrite and compete with their epibiotic bacteria for this Fe source. To study this complex system, we carefully optimized a radiotracer method ensuring complete removal of external ferrihydrite and efficient separation of bacteria from the colonies. Trichodesmium‐only uptake rates of natural colonies were 5–50 times faster than those of laboratory culture, suggesting that natural colonies acquire ferrihydrite at a greater efficiency. In some days, total uptake rates of natural colonies exceeded dissolved Fe release from ferrihydrite, indicating that the colonies enhance the mineral dissolution rate. Furthermore, uptake rates of bacteria associated with natural colonies were faster than those of bacteria associated with the culture, implying that the bacteria benefit from the Trichodesmium‐enhanced mineral dissolution. At the cellular level, surface area normalized uptake rates of bacteria always exceeded those of cultured Trichodesmium, but in natural populations, the dominance shifted between Trichodesmium and bacteria on different days. At the community level, when accounting for the total bacteria and Trichodesmium cells, Trichodesmium dominated Fe uptake in both cultured and natural colonies. Overall, our findings suggest that natural Trichodesmium colonies are exceptionally adapted for accessing mineral Fe and maintaining a sustainable relationship with their associated bacteria.

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

“…In a first approach, we added two different bacterial strains originally isolated from Trichodesmium in Eilat (Basu et al ) to freshly collected colonies. While the initial abundance of (naturally occurring) bacteria in these colonies could not be quantified, we assumed a similar abundance as during a comparable sampling campaign at the same location (7.5 ± 0.46 × 10 4 cells colony −1 ; Basu and Shaked ). The amount of bacteria ultimately incorporated into the colony after their addition and subsequent 30–60 min incubation likely depends on whether they preferentially resided in the colony microenvironment, which can be facilitated by motility and chemotactic behavior (e.g., Stocker and Seymour ).…”

“…( c ) Estimated bacterial O 2 uptake at naturally relevant numbers of bacteria per colony, extrapolated from data shown in panel ( b ) (linear regression integrated for E23 and E6, with y‐axis intercept set to 0). The range of bacterial densities observed in natural Trichodesmium colonies in Eilat (Basu and Shaked ) is indicated by blue shading. Average O 2 uptake by natural colonies measured in the dark (this study) is indicated by the arrow on the y‐axis.…”

“…We hence applied the relationship between O 2 uptake rate and bacterial density that was determined in agar spheres to estimate the contribution of bacteria to total O 2 uptake by the colony consortium. Since the bacterial densities previously determined in Trichodesmium colonies from the Gulf of Eilat of 5–11 × 10 4 cells colony −1 (Basu and Shaked ) are below those tested in the agar sphere experiments (Fig. b), we extrapolated the bacterial O 2 uptake rates to naturally relevant bacterial densities (Fig.…”

“…After 3–12 h, incubations were stopped by filtering colonies on 8 μ m polycarbonate filters. Extracellular iron as well as attached bacteria were subsequently removed by a thorough wash in Ti‐EDTA‐citrate solution (as described by Basu and Shaked ) before determination of internalized 55 Fe (Tri‐carb 1600 CA scintillation counter, Packard).…”

“…Trichodesmium colonies in the Gulf of Eilat were recently shown to harbor a range of siderophore‐producing bacteria (Basu et al ; Gledhill et al ), and addition of siderophores to natural colonies enhanced the dissolution as well as the uptake of mineral‐bound iron by both Trichodesmium and associated bacteria (Basu et al ). Taken together, these findings suggest that the close proximity of Trichodesmium cells, bacteria, and dust within colonies allows for efficient ligand‐promoted dissolution and transfer of iron to Trichodesmium (Basu and Shaked ; Basu et al ).…”