Trichodesmium physiological ecology and phosphate reduction in the western tropical South Pacific

Abstract

N2 fixation by the genus Trichodesmium is predicted to support a large proportion of the primary productivity across the oligotrophic oceans, regions that are considered among the largest biomes on Earth. Many of these environments remain poorly sampled, limiting our understanding of Trichodesmium physiological ecology in these critical oligotrophic regions. Trichodesmium colonies, communities that consist of the Trichodesmium host and their associated microbiome, were collected across the oligotrophic western tropical South Pacific (WTSP). These samples were used to assess host clade distribution, host and microbiome metabolic potential, and functional gene expression, with a focus on identifying Trichodesmium physiological ecology in this region. Genes sets related to phosphorus, iron, and phosphorus–iron co-limitation were dynamically expressed across the WTSP transect, suggestive of the importance of these resources in driving Trichodesmium physiological ecology in this region. A gene cassette for phosphonate biosynthesis was detected in Trichodesmium, the expression of which co-varied with the abundance of Trichodesmium Clade III, which was unusually abundant relative to Clade I in this environment. Coincident with the expression of the gene cassette, phosphate reduction to phosphite and low-molecular-weight phosphonate compounds was measured in Trichodesmium colonies. The expression of genes that enable use of such reduced-phosphorus compounds were also measured in both Trichodesmium and the microbiome. Overall, these results highlight physiological strategies employed by consortia in an undersampled region of the oligotrophic WTSP and reveal the molecular mechanisms underlying previously observed high rates of phosphorus reduction in Trichodesmium colonies.