Auxin production in the green alga Chlamydomonas involves an extracellular L-amino acid oxidase and supports algal-bacterial mutualism with methylobacteria

Abstract

Interactions between algae and bacteria are widespread in aquatic and terrestrial ecosystems and play fundamental roles in nutrient cycling and biomass production. However, the chemical basis for many of these interactions is poorly characterized and understood. Recent studies have shown that the plant auxin indole acetic acid (IAA) can mediate chemical crosstalk between algae and bacteria, resembling its role in plant-bacterial associations. While algae have been shown to produce IAA, molecular pathways for IAA synthesis in algae have remained elusive. Here, we report a mechanism for IAA production from L-tryptophan mediated by the extracellular enzyme L-amino acid oxidase (LAO1) in the model alga Chlamydomonas reinhardtii. Under inorganic nitrogen limitation but in the presence of L-tryptophan and other amino acids, high levels of IAA are generated in an LAO1-dependent manner. Thus, LAO1 plays a dual role in scavenging nitrogen from L-amino acids and in producing the phytohormone IAA, which subsequently inhibits algal cell multiplication and chlorophyll degradation. We show that these inhibitory effects can be relieved in the presence of Methylobacterium spp., well-known plant growth-promoting bacteria (PGPB), whose growth is mutualistically enhanced by the presence of the alga. These findings reveal a complex interplay of microbial auxin production and degradation by algal-bacterial consortia under nitrogen limitation and draws attention to potential ecophysiological roles of terrestrial microalgae and PGPB in association with land plants.

<em>Chlamydomonas Reinhardtii, </em>a Reference Organism to Study Algal-Microbial Interactions. <em>Why Can’t They Be Friends</em>

“…can break down amino acids and peptides to feed Chlamydomonas with ammonium in exchange for the photosynthate glycerol [87]. Additionally, auxin produced by Chlamydomonas can feed Methylobacterium aquaticum, which in turn promotes algal growth [99]. Lastly, N2-fixing bacteria like Azotobacter chroococcum, A. beljerinckii, A. agilis and A. vinelandii can support Chlamydomonas growth with fixed nitrogen in exchange for fixed carbon [65,[67][68][69]71].…”

“…Since both Chlamydomonas and Methylobacterium spp. are found in the rhizosphere, this chemical crosstalk mediated by auxin production and degradation may impact plant fitness and could be used to improve crop yields in sustainable agriculture [99].…”