A denitrifying community associated with a major, marine nitrogen fixer

Abstract

SummaryThe diazotrophic cyanobacterium, Trichodesmium, is an integral component of the marine nitrogen cycle and contributes significant amounts of new nitrogen to oligotrophic, tropical/subtropical ocean surface waters. Trichodesmium forms macroscopic, fusiform (tufts), spherical (puffs) and raft-like colonies that provide a pseudobenthic habitat for a host of other organisms including marine invertebrates, microeukaryotes and numerous other microbes. The diversity and activity of denitrifying bacteria found in association with the colonies was interrogated using a series of molecular-based methodologies targeting the gene encoding the terminal step in the denitrification pathway, nitrous oxide reductase (nosZ). Trichodesmium spp. sampled from geographically isolated ocean provinces (the Atlantic Ocean, the Red Sea and the Indian Ocean) were shown to harbor highly similar, taxonomically related communities of denitrifiers whose members are affiliated with the Roseobacter clade within the Rhodobacteraceae (Alphaproteobacteria). These organisms were actively expressing nosZ in samples taken from the mid-Atlantic Ocean and Red Sea implying that Trichodesmium colonies are potential sites of nitrous oxide consumption and perhaps earlier steps in the denitrification pathway also. It is proposed that coupled nitrification of newly fixed N is the most likely source of nitrogen oxides supporting nitrous oxide cycling within Trichodesmium colonies.

Spatial Variability and Co-acclimation of Phytoplankton and Bacterioplankton Communities in the Pearl River Estuary, China

“…An unclassified bacterial group of the family Rhodobacteraceae contained the genes nirB, nirD, nirK, narG, nasA, narl, norC, napA, nifD, nifK, nifH, norB , and hcp and was the dominant bacterial phylotype in the mesohaline water at site S7. Bacteria affiliated with Rhodobacteraceae have been acknowledged to play significant roles in the nitrogen cycle ( Coates and Wyman, 2017 ). Previous studies have demonstrated that Roseobacter , affiliated with Rhodobacteraceae, can rapidly assimilate ammonium and use dissolved organic nitrogen (DON) as a N source ( Mayali et al, 2014 ).…”

Processes and Microorganisms Involved in the Marine Nitrogen Cycle: Knowledge and Gaps

“…Denitrification also occurs in other niches outside anoxic sediments and OMZs. For example, the lowoxygen environment within Trichodesmium colonies allows the growth of active denitrifiers harboring nosZ genes, representing a potential sink for N 2 O within oceanic surface waters (Wyman et al, 2013;Coates and Wyman, 2017). Diverse bacteria harboring nir genes have been also found in corals and sponges (Hoffmann et al, 2009;Yang et al, 2013).…”

Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies

“…Complete denitrification was not detectable, presumably due to the low nitrate availability and high oxygen concentrations (≥50% air-saturation or ≥100 µM) even during darkness. Denitrifiers and denitrification-relevant gene expression (nosZ) have been shown to be present in natural Trichodesmium colonies [14,87]. However, most denitrifiers are facultative aerobes/anaerobes, depending on oxygen and nitrate availabilities [88].…”

“…Trichodesmium grows as filaments, referred to as trichomes, which at times aggregate as millimetre-sized spindle-shaped (tufts) or spherical (puffs) colonies [10], often forming conspicuous blooms which can be observed from space [11]. These colonies have long been recognised as hot spots for N 2 fixation [12,13] but are increasingly suspected to host additional processes including N recycling and loss processes, as inferred from nucleic acid analyses [14][15][16].…”

“…Metagenomic studies showed that epibionts substantially expand the metabolic functionality in colonies compared to single trichomes [38]. With respect to N pathways, transcripts encoding for ammonium, nitrite and nitrate transporters, and for genes involved in assimilatory/ dissimilatory nitrate reduction to ammonium and denitrification have been detected [14][15][16]. Thus, the metabolic potential of the Trichodesmium holobiont stretches beyond N 2 fixation, suggesting an intimate spatial coupling of various N cycling processes.…”