The Symbiotic “All-Rounders”: Partnerships between Marine Animals and Chemosynthetic Nitrogen-Fixing Bacteria

Abstract

Nitrogen fixation is a widespread metabolic trait in certain types of microorganisms called diazotrophs. Bioavailable nitrogen is limited in various habitats on land and in the sea, and accordingly, a range of plant, animal, and single-celled eukaryotes have evolved symbioses with diverse diazotrophic bacteria, with enormous economic and ecological benefits. Until recently, all known nitrogen-fixing symbionts were heterotrophs such as nodulating rhizobia, or photoautotrophs such as cyanobacteria. In 2016, the first chemoautotrophic nitrogen-fixing symbionts were discovered in a common family of marine clams, the Lucinidae. Chemosynthetic nitrogen-fixing symbionts use the chemical energy stored in reduced sulfur compounds to power carbon and nitrogen fixation, making them metabolic ‘all-rounders’ with multiple functions in the symbiosis. This distinguishes them from heterotrophic symbionts that require a source of carbon from their host, and their chemosynthetic metabolism distinguishes them from photoautotrophic symbionts that produce oxygen, a potent inhibitor of nitrogenase. In this review, we consider evolutionary aspects of this discovery, by comparing strategies that have evolved for hosting intracellular nitrogen-fixing symbionts in plants and animals. The symbiosis between lucinid clams and chemosynthetic nitrogen-fixing bacteria also has important ecological impacts, as they form a nested symbiosis with endangered marine seagrasses. Notably, nitrogen fixation by lucinid symbionts may help support seagrass health by providing a source of nitrogen in seagrass habitats. These discoveries were enabled by new techniques for understanding the activity of microbial populations in natural environments. However, an animal (or plant) host represents a diverse landscape of microbial niches due to its structural, chemical, immune and behavioural properties. In future, methods that resolve microbial activity at the single cell level will provide radical new insights into the regulation of nitrogen fixation in chemosynthetic symbionts, shedding new light on the evolution of nitrogen-fixing symbioses in contrasting hosts and environments.

Adaptations to nitrogen availability drive ecological divergence of chemosynthetic symbionts

“…The coastal waters of the TEP are frequently enriched with nutrients due to seasonal upwelling, leading to nitrate levels that are roughly ten times higher than those found in seagrass beds in the Caribbean [ 31 , 32 ]. Hence, the absence of nitrogen fixation genes in the symbiont MAGs from the nitrogen-rich TEP region is consistent with the hypothesis that lucinid symbiont diazotrophy has evolved as an adaptation to life in nitrogen-poor oligotrophic habitats like tropical coral reefs and seagrass beds [ 33 ]. Although the TEP symbionts did not possess the capacity to fix nitrogen, the MAGs of all three TEP symbiont lineages encoded unique accessory metabolic capabilities that were lacking in the Caribbean symbionts.…”

Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of a salt marsh foundation plant species

“…We show that our MAGs formed a monophyletic clade with those from previously described marine invertebrate animals (Figure 4). Similar to what has been reported in their symbiosis with lucinid (Petersen and Yuen, 2021). Furthermore, invertebrate colonization by Ca.…”

Sulfur oxidation and reduction are coupled to nitrogen fixation in the roots of the salt marsh foundation plant Spartina alterniflora

“…Studies of lucinid clams have shown that the Ca . Thiodiazotropha symbionts are horizontally transmitted 48 . Furthermore, invertebrate colonization by Ca .…”