Iron and phosphorus deprivation induce sociality in the marine bloom-forming cyanobacterium Trichodesmium

Abstract

Trichodesmium spp. are diazotrophic cyanobacteria that exist as single filaments (trichomes) and as macroscopic colonies of varying shapes formed by aggregating trichomes. The causes and dynamics of colony formation and disassociation are not yet elucidated. we demonstrate that limited availability of dissolved phosphorus (P) or iron (Fe) stimulated trichome mobility and induced colony formation in Trichodesmium erythraeum IMS101 cultures. The specific nutrient limitation differentially affected the rate of colony formation and morphology of the colonies. Fe starvation promoted rapid colony formation (10-48 h from depletion) while 5-7 days were required for colonies to form in P-depleted cultures. Video analyses confirmed that the probability of trichomes to cluster increased from 12 to 35% when transferred from nutrient replete to Fe-depleted conditions. Moreover, the probability for Fe-depleted aggregates to remain colonial increased to 50% from only 10% in nutrient replete cultures. These colonies were also characterized by stronger attachment forces between the trichomes. Enrichment of nutrient-depleted cultures with the limited nutrient-stimulated colony dissociation into single trichomes. We postulate that limited P and Fe availability enhance colony formation of Trichodesmium and primarily control the abundance and distribution of its different morphologies in the nutrient-limited surface ocean.

Interactions between ultraviolet radiation exposure and phosphorus limitation in the marine nitrogen‐fixing cyanobacteria Trichodesmium and Crocosphaera

“…Our culture study suggests that Trichodesmium IMS 101 may use this protective strategy of adopting a colonial morphotype to help counteract inhibitory UV levels. This is consistent with a recent study by Tzubari et al (), who found that Trichodesmium IMS101 grew as single filaments during exponential growth, but formed colonies under oxidative stress or when limited by Fe or P. Although both IMS 101 and GBR died after several days under the highest UV‐B radiation treatment (1 W m −2 ), GBR did not use this potentially protective colonial strategy.…”

N2 fixation in free‐floating filaments of Trichodesmium is higher than in transiently suboxic colony microenvironments

“…By contrast with a recent laboratory study by Tzubari et al . (), we therefore assumed that, in our experiment, colony formation was not induced by P‐ or Fe‐depletion. As we did not observe any differences in abiotic conditions or cellular composition between free‐floating trichomes and colonies, the triggers for colony formation could not be identified.…”

Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies

“…Thus, Trichodesmium cells (and its epibionts) appeared to act in concert to preserve new N from N 2 fixation in close proximity, to fully benefit from bioavailable N in the oligotrophic near-surface ocean. Trichodesmium colonies may thus be described as consortia, reflecting associations of synergistic, mutualistic or syntrophic lifestyles [99,100], in which the growth and elemental cycling are more efficient than on a single-population level.…”