Trichodesmium– a widespread marine cyanobacterium with unusual nitrogen fixation properties

Abstract

The last several decades have witnessed dramatic advances in unfolding the diversity and commonality of oceanic diazotrophs and their N2-fixing potential. More recently, substantial progress in diazotrophic cell biology has provided a wealth of information on processes and mechanisms involved. The substantial contribution by the diazotrophic cyanobacterial genus Trichodesmium to the nitrogen influx of the global marine ecosystem is by now undisputable and of paramount ecological importance, while the underlying cellular and molecular regulatory physiology has only recently started to unfold. Here, we explore and summarize current knowledge, related to the optimization of its diazotrophic capacity, from genomics to ecophysiological processes, via, for example, cellular differentiation (diazocytes) and temporal regulations, and suggest cellular research avenues that now ought to be explored.

Programmed cell death in the marine cyanobacterium Trichodesmium mediates carbon and nitrogen export

“…After B3 h, 96-98% of the cells had concentrated at the surface, incorporating significant concentrations of TOC and total organic N (0.72 ± 0.09 mg C m À 2 and 0.13 ± 0.03 mg N m À 2 , respectively), whereas o2% of the cells were evenly distributed below the upper 0.5 cm throughout the rest of the water column (Figure 2a). Although artificially expedited using dense batch cultures (Figure 1), bloom formation in our water column possessed notable similarities to natural blooms observed in tropical oceans, where surface slicks of dense Trichodesmium aggregations develop under calm conditions with sea surface temperatures of ± 26 1C, high solar irradiance and high concentrations of Fe and P (Karl et al, 2002;Le Borgne, 2008, 2010;Bergman et al, 2012). In these oceanic blooms, the vertical ascent of Trichodesmium cells due to positive buoyancy (Villareal and Carpenter, 2003;Le Borgne, 2008, 2010) occurs simultaneously with rapid growth rates, both processes accounting for the hastened, ultra-dense accumulation of cells at the surface Le Borgne, 2008, 2010;Bergman et al, 2012).…”

“…The mechanistic link between PCD cellular processes and associated pulses of C:N export underscores its fundamental role in regulating cell fate, particle flux, and upper ocean biogeochemistry of bloom-forming diazotrophs. Although export fluxes from natural Trichodesmium or other diazotrophic blooms are poorly defined (Mulholland, 2007;Bergman et al, 2012), newly fixed particulate organic matter (POM) in the pelagic surface oceans is the primary source for exported C and N to the deep ocean (Buesseler et al, 2007;Arístegui et al, 2009). Globally, the export efficiency of POM from surface waters via the biological pump varies considerably (from 2 to 50%), with up to a quarter of this material sinking below 1000 m , depending on the magnitude of net primary production, sinking velocities and remineralization rates De La Rocha and Passow, 2007).…”

“…These blooms develop swiftly and are characterized by high rates of CO 2 and N 2 fixation, up to 640 pg C per cell per day and 29 pg N per cell per day, respectively, as well as rapid doubling times (B2.6 day) (Capone et al, 1998;Le Borgne, 2008, 2010;Luo et al, 2012). The elicitors and signals causing these rapid surface-bloom formations of Trichodesmium are still vague (Berman-Frank et al, 2007;Rodier and Le Borgne, 2010;Bergman et al, 2012).…”

“…Notably, these massive Trichodesmium blooms often collapse abruptly (within 3-5 days), with mortality rates paralleling bloom development rates Le Borgne, 2008, 2010;Bergman et al, 2012) and with different processes (not necessarily mutually exclusive in natural populations) being implicated in their termination. Bloom crashes may result from viral lysis (Hewson et al, 2004) or autocatalytic programmed cell death (PCD), which is induced by nutrient (iron (Fe) starvation) or high light (oxidative) stress in both laboratory and natural populations (Berman-Frank et al, 2004, 2007.…”

“…Indeed, the fate and quantitative contribution of Trichodesmium blooms to the vertical export or recycling of newly fixed nitrogen (N) and carbon (C) in the ocean following bloom collapse is poorly studied (Mulholland, 2007;Bergman et al, 2012), despite its global-scale importance Tg N per year and 2.1-18 Tg C per year) (Luo et al, 2012). Trichodesmium may release up to 50-80% of recently fixed N 2 in natural communities and cultures as dissolved organic N and ammonium (NH 4 þ ) (Mulholland, 2007).…”