The Ecology of Reoccurring Associations Between Eukaryotic Phytoplankton and the Nitrogen-Fixing Cyanobacterium, Trichodesmium

Abstract

Nitrogen is one of the basic elements of life; however, throughout much of the surface waters of the world’s oceans, inorganic nitrogen substrates (e.g., ammonium, nitrate or nitrite) are found in very low concentrations. A select group of organisms, diazotrophs, are able to assimilate nitrogen from the nearly inexhaustible pool of atmospheric nitrogen gas (N2) by reducing N2 to biologically available forms. Our research focused on a specific association between the N2-fixing cyanobacterium Trichodesmium and eukaryotic phytoplankton, specifically various genera of diatoms. Both Trichodesmium and diatoms can be important contributors to biogeochemical cycling in the subtropical North Pacific Ocean, including playing key roles in influencing export of various bioelements to the deep sea. Based on initial microscopic observations, we hypothesized that a symbiotic interaction between specific types of diatoms and Trichodesmium spiralis play an important role in carbon and nitrogen cycling at Station ALOHA, the field site for the Hawaii Ocean Time-series program, located approximately 100 km north of the island of O‘ahu, Hawai‘i. Microscopic examination of upper ocean (0-175 m) seawater samples collected at near-monthly time scales over 8 months revealed that T. spiralis was most abundant in the well-lit upper 75 m, but that the prevalence of diatoms with T. spiralis did not demonstrate depth- or time-dependent patterns. Amplification and sequencing of diatom rbcL genes, the gene encoding the large subunit of the RuBisCo enzyme, from handpicked T. spiralis colonies revealed three major phylotypes of diatoms: two phylotypes clustered within diatoms belonging to the genus Cylindrotheca and one phylotype was phylogenetically closely related to diatoms belonging to the genus Rhopalodia. In addition, confocal and scanning electron microscopy were used to visualize the physical association between T. spiralis and the diatoms. Collectively, our results provide the first description of a reoccurring association between two important groups of phytoplankton, with significant implications for the cycling of nutrient and carbon in the subtropical North Pacific Ocean.