A denitrifying community associated with a major, marine nitrogen fixer.

Christopher J Coates,Michael Wyman

doi:10.1111/1462-2920.14007

Abstract

The 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.

Highlights

It is over twenty years since Louis Codispoti posed the question ‘Are the oceans losing nitrate?’ (Codispoti, 1995)
Heterotrophic activity associated with these organically rich microenvironments can reduce internal oxygen tensions sufficiently to enable oxygen-sensitive processes to proceed, as has been demonstrated recently for both denitrification and N fixation in association with copepods (Glud et al, 2015; Scavotto et al, 2015). Earlier work from this laboratory showed that the colonial cyanobacterium, Trichodesmium, harbors denitrifying bacteria (Wyman et al, 2013): a finding that hints at a more intimate spatial coupling of oceanic nitrogen sources and sinks than that envisaged by current models of ocean geochemistry (Deutsch et al, 2007)
Preliminary experiments with Trichodesmium samples originating from the Arabian Sea showed that while nosZ could be amplified routinely from gDNA extracted from the colonies tested, the overall diversity of the amplicons retrieved was low when their DNA sequences were compared

Summary

The 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 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 .

Introduction

Results and discussion

Experimental procedures