Fe and P Limitation Induce Sociality in the Marine Cyanobacterium Trichodesmium

Trichodesmium spp. are filamentous, non-heterocystous, cyanobacteria that exist as single filaments (trichomes) and as macroscopic colonies. Colonies are well described, yet the causes and dynamics of colony formation and disassociation are not yet elucidated. We demonstrate that in Trichodesmium IMS101 cultures limited availability of dissolved phosphorus (P) or iron (Fe) stimulates trichome mobility and induces colony formation. The specific nutrient limitation further affected the rate and morphology of colony formation with Fe-starvation promoting rapid colony formation (within 10-24 h from depletion) compared to 5-7 d in P-depleted cultures. Video analyses confirmed that the probability of trichomes to cluster, and remain colonial, increased from 10-25% in nutrient-replete to 50-90% in Fe-depleted cultures. Fe-depleted cultures were further characterized by stronger attachment forces between the trichomes, due to enhanced excretion of transparent extracellular polysaccharide mucus. Culture enrichment with the limited nutrient stimulated colony dissociation into single trichomes and confirmed that nutrient stress in Trichodesmium prompts social interactions of trichomes leading to colonial morphologies. We postulate that the abundance and distribution of the different Trichodesmium morphologies in the ocean are primarily controlled by P and Fe availability that prompt sociality and colony formation. Moreover, the colonial morphology, and its associated epibiont activity, enhance the colony’s selective advantage and persistence in the dynamic oceans and impact its fate and the biogeochemical cycling of nutrients.