Nitrogen fixation in eukaryotes – New models for symbiosis

Abstract

BackgroundNitrogen, a component of many bio-molecules, is essential for growth and development of all organisms. Most nitrogen exists in the atmosphere, and utilisation of this source is important as a means of avoiding nitrogen starvation. However, the ability to fix atmospheric nitrogen via the nitrogenase enzyme complex is restricted to some bacteria. Eukaryotic organisms are only able to obtain fixed nitrogen through their symbiotic interactions with nitrogen-fixing prokaryotes. These symbioses involve a variety of host organisms, including animals, plants, fungi and protists.ResultsWe have compared the morphological, physiological and molecular characteristics of nitrogen fixing symbiotic associations of bacteria and their diverse hosts. Special features of the interaction, e.g. vertical transmission of symbionts, grade of dependency of partners and physiological modifications have been considered in terms of extent of co-evolution and adaptation. Our findings are that, despite many adaptations enabling a beneficial partnership, most symbioses for molecular nitrogen fixation involve facultative interactions. However, some interactions, among them endosymbioses between cyanobacteria and diatoms, show characteristics that reveal a more obligate status of co-evolution.ConclusionOur review emphasises that molecular nitrogen fixation, a driving force for interactions and co-evolution of different species, is a widespread phenomenon involving many different organisms and ecosystems. The diverse grades of symbioses, ranging from loose associations to highly specific intracellular interactions, might themselves reflect the range of potential evolutionary fates for symbiotic partnerships. These include the extreme evolutionary modifications and adaptations that have accompanied the formation of organelles in eukaryotic cells: plastids and mitochondria. However, age and extensive adaptation of plastids and mitochondria complicate the investigation of processes involved in the transition of symbionts to organelles. Extant lineages of symbiotic associations for nitrogen fixation show diverse grades of adaptation and co-evolution, thereby representing different stages of symbiont-host interaction. In particular cyanobacterial associations with protists, like the Rhopalodia gibba-spheroid body symbiosis, could serve as important model systems for the investigation of the complex mechanisms underlying organelle evolution.

The dynamics of microbial partnerships in the coral Isopora palifera

“…Nitrogen-fixing bacteria have been detected elsewhere in coral (Shashar et al, 1994;Lesser et al, 2004). In this study, we also detected several potential nitrogen fixers, including Cyanobacteria (Meeks, 1998;Berman-Frank et al, 2003), Clostridia (Chen et al, 2001), Chlorobia (Wahlund and Madigan, 1993) and Chloroflexi (Seshadri et al, 2005;Kneip et al, 2007). These potential nitrogen fixer groups in I. palifera greatly were enriched in February and April ( Figure 5).…”

Nitrogen fixation in a chemoautotrophic lucinid symbiosis

“…2) with an average ethylene production rate of 43 nmol h −1 mg −1 under aerobic conditions. Under microaerobic conditions, the nitrogenase activity of purified symbionts was even higher (57.5 nmol C 2 H 4 h −1 mg −1 ) than in the aerobic approach, suggesting that the thioautotrophic symbiont's nitrogenase enzyme complex may-as most other nitrogenases-be oxygen-sensitive and work more efficiently under low-oxygen conditions 16 . Low ethylene production (∼0.24 nmol C 2 H 4 h −1 mg −1 ) was observed in crude sediment collected from T. testudinum seagrass beds, presumably indicating the presence of free-living nitrogen-fixing bacteria in the sediment.…”

“…It provides the basis for the biosynthesis of organic nitrogen compounds and thus of indispensable cellular components such as proteins and nucleic acids. Diazotrophy occurs exclusively in the prokaryotic kingdom 15 ; nitrogen fixation in eukaryotes is therefore restricted to symbioses with bacteria 16 . Prokaryotic nitrogen fixers are associated with a diversity of eukaryotic hosts in a wide range of habitats, including the well-studied Rhizobium and Bradyrhizobium genera that form root-nodule symbioses with legumes 17 and the actinomycetal Frankia species associated with woody plants 18 .…”

Diversity of foliar endophytic fungi from the medicinal plant Sapindus saponaria L . and their localization by scanning electron microscopy

“…In that regard, we note that intracellular colonization of leaves by fungal endophytes indicates a high interaction between them, positively selected in a coevolutionary event. Kneip et al (2007), discussing new models for symbiosis, compared the morphological, physiological and molecular characteristics of nitrogen fi xing symbiotic associations of bacteria and their diverse hosts. Special features of the interaction, e.g.…”