Colonies of the marine cyanobacterium Trichodesmium optimize dust utilization by selective collection and retention of nutrient-rich particles

Abstract

Trichodesmium, a globally important, N₂-fixing, and colony-forming cyanobacterium, employs multiple pathways for acquiring nutrients from air-borne dust, including active dust collection. Once concentrated within the colony core, dust can supply Trichodesmium with nutrients. Recently, we reported a selectivity in particle collection enabling Trichodesmium to center iron-rich minerals and optimize its nutrient utilization. In this follow-up study we examined if colonies select Phosphorus (P) minerals. We incubated 1,200 Trichodesmium colonies from the Red Sea with P-free CaCO₃, P-coated CaCO₃, and dust, over an entire bloom season. These colonies preferably interacted, centered, and retained P-coated CaCO₃ compared with P-free CaCO₃. In both studies, Trichodesmium clearly favored dust over all other particles tested, whereas nutrient-free particles were barely collected or retained, indicating that the colonies sense the particle composition and preferably collect nutrient-rich particles. This unique ability contributes to Trichodesmium's current ecological success and may assist it to flourish in future warmer oceans.

Keywords: Ecology; Geomicrobiology; Microbiology.

Graphical abstract

Figure 1

Characterization scheme of colony-particle interactions Characterization of colony-particle interactions during three time points, representing three different parameters. A score and color-code was assigned for each parameter according to the criteria shown, following the criteria of Kessler et al. (2020a) with some modifications. Scores were assigned to alive and integral colonies.

Figure 2

Single colony index The integration of all three scored interaction parameters assigned to each colony (Figure 1) into a single value describing the colony-particle interaction over time. From all 27 possible combinations of the three interaction parameters, 12 common patterns were found to represent ∼90% of the colonies during the incubation experiments. These 12 patterns are further grouped into four categories ranked and color-coded according to the strength of colony-particle interactions.

Figure 3

Interactions between natural Trichodesmium colonies and P-free or P-rich CaCO₃ in an experiment conducted on October 28, 2019 (A) Short-term (ST) interactions, (B) Centering, and (C) Long-term (LT) interactions (see Figure 1). Pictures of colonies with particles representing each parameter score are shown next to each panel. Statistically significant differences between particle types (p < 0.05) were found for all parameters, as labeled by letters. Natural colonies preferably interacted, centered, and retained P-rich particles in comparison with P-free particles.

Figure 4

Interactions between natural Trichodesmium colonies and P-free or P-rich CaCO₃ particles over the entire season as characterized by discrete parameters (A) and single colony index (B) (A) Short-term (ST) interactions, Centering, and Long-term (LT) interactions (see Figure 1). (B) Fraction of colonies per single-colony index category over the entire season (Figure 2). The color-coded categories are ordered at increasing interaction strength with “inactive” on the left and “very active” on the right. Hatched and solid bars represent P-free and P-rich CaCO₃ treatments, respectively. Numbers above each bar graph represent the total colony number in each category. A preference for P-rich CaCO₃ is seen by a higher abundance of colonies showing active patterns in the P-rich CaCO₃ treatment compared with the P-free CaCO₃ treatment.

Figure 5

Daily colony-particle interactions throughout the season presented using the single colony index Day-to-day and seasonal variations of a colony's tendency to interact with particles (interaction strength) and preference for P-rich particles (selectivity). A high abundance of active colonies can be seen in late season (November 7–19) compared with more inactive colonies early in the season (October 7–November 7). Top (A) and bottom (B) panels represent P-free and P-rich CaCO₃ treatments, respectively. Bars do not reach 100% as the missing fraction represents minor patterns that are not grouped into the four chosen categories.

Figure 6

Factors influencing the day-to-day variability in colony-particle interactions (A) Separation of thin (left) and dense (right) morphotypes on November 17 and 19 demonstrates differences of a colony's tendency to interact with particles (interaction strength) and preference for P-rich particles (selectivity) according to morphotype. Interaction strength is based on the single colony index categories, whereas selectivity is based on differences between the inner (P-free CaCO₃) and outer (P-rich CaCO₃) circles. In general, thin morphotypes were more interactive (interaction strength) and showed more selectivity for particles in comparison with the dense morphotypes. (B) Relative expressions of P stress marker gene sphX in natural colonies, collected on November 6, in situ (T₀) and after 24 h incubations without PO₄³⁻ (T_24-P) and with 5 μM PO₄³⁻ (T_24+P). The lower transcription of sphX gene transcription for T_24+P in comparison with T₀ and T_24-P indicates that the collected colonies were P-limited. Error bars represent the standard deviation (n = 2). (C) Relative expressions of sphX in natural colonies, collected in situ for 6 days throughout the season (including November 6). Colonies collected on October 27 and November 3 were presumably P-limited owing to similar sphX expression in comparison with November 6. Error bars represent the standard deviation (n = 2).

Figure 7

Summary of colony-particle interactions observed in this study for all tested mineral types (P-free CaCO₃, P-rich CaCO₃, and mineral dust) according to the single colony index categories Collectively a total of 1,104 colonies were characterized in this study and 962 colonies following common patterns were presented above. Colonies show a strong preference for dust over P-rich CaCO₃ as well as discrimination against P-free CaCO₃.

Figure 8

Contrasting colony-particle interaction days Three days with contrasting colony-particle interaction strength to demonstrate variations in a colony's tendency to interact with particles (interaction strength) and preference for P-rich particles (selectivity). Interaction strength is based on the single colony index categories, whereas selectivity is based on differences between the inner (P-free CaCO₃) and outer (P-rich CaCO₃) circles.

Figure 9

Compilation of Trichodesmium colony-particle interaction studies We combine the current study data with that of Kessler et al. (2020a), by plotting the percentage of colonies interacting with particles initially (ST) and after overnight incubation (LT). Nutrient-free particles (CaCO₃, quartz, diatom frustule, and acid-cleaned dust) are plotted as empty symbols, nutrient-rich particles appear as colored symbols, and dust appear as black circles. A clear selection can be seen among different mineral types, where the cartoon on the right highlight's key trends from the data.