Indole-3-Acetic Acid Is Produced by Emiliania huxleyi Coccolith-Bearing Cells and Triggers a Physiological Response in Bald Cells

Abstract

Indole-3-acetic acid (IAA) is an auxin produced by terrestrial plants which influences development through a variety of cellular mechanisms, such as altering cell orientation, organ development, fertility, and cell elongation. IAA is also produced by bacterial pathogens and symbionts of plants and algae, allowing them to manipulate growth and development of their host. They do so by either producing excess exogenous IAA or hijacking the IAA biosynthesis pathway of their host. The endogenous production of IAA by algae remains contentious. Using Emiliania huxleyi, a globally abundant marine haptophyte, we investigated the presence and potential role of IAA in algae. Homologs of genes involved in several tryptophan-dependent IAA biosynthesis pathways were identified in E. huxleyi. This suggests that this haptophyte can synthesize IAA using various precursors derived from tryptophan. Addition of L-tryptophan to E. huxleyi stimulated IAA production, which could be detected using Salkowski's reagent and GC × GC-TOFMS in the C cell type (coccolith bearing), but not in the N cell type (bald). Various concentrations of IAA were exogenously added to these two cell types to identify a physiological response in E. huxleyi. The N cell type, which did not produce IAA, was more sensitive to it, showing an increased variation in cell size, membrane permeability, and a corresponding increase in the photosynthetic potential quantum yield of Photosystem II (PSII). A roseobacter (bacteria commonly associated with E. huxleyi) Ruegeria sp. R11, previously shown to produce IAA, was co-cultured with E. huxleyi C and N cells. IAA could not be detected from these co-cultures, and even when stimulated by addition of L-tryptophan, they produced less IAA than axenic C type culture similarly induced. This suggests that IAA plays a novel role signaling between different E. huxleyi cell types, rather than between a bacteria and its algal host.

Dynamic metabolic exchange governs a marine algal-bacterial interaction

“…The results of our experiments indicate that all produced IAA is fully labeled (Figure 5b), thus indicating that exogenous tryptophan is directly converted to IAA. Of note, a recent study reported on the production of IAA in the mM range in axenic E. huxleyi cultures supplemented with tryptophan (Labeeuw et al, 2016). As all of our experiments and controls indicated no IAA production by algae, currently we do not understand the source of this apparent contradiction.

10.7554/eLife.17473.008Figure 5.Exogenous tryptophan promotes bacterial IAA biosynthesis.( a ) Addition of 0.1 mM tryptophan to P. inhibens cultures results in approximately 25-fold increase in produced IAA.

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The Bacterial Symbiont Phaeobacter inhibens Shapes the Life History of Its Algal Host Emiliania huxleyi

“…However, Segev et al (2016) also showed that P. inhibens did not produce IAA at high enough concentrations to kill E. huxleyi CCMP3266 (0.4-10 nM). In addition, E. huxleyi CCMP3266 produces IAA itself as a cell-cell signal at a higher concentration (200 µM) in the presence of tryptophan (Labeeuw et al, 2016). Finally, the Ntype strain, CCMP2090, is susceptible to IAA when co-cultured at lower concentrations (10-100 µM), exhibiting morphological responses and reduced health similar to those seen in terrestrial plants (Labeeuw et al, 2016) that we did not observe in the P. inhibens-CCMP2090 co-culture.…”

“…Segev et al (2016) has proposed that P. inhibens uses IAA to kill E. huxleyi. This plant auxin is produced by various roseobacters (Fernandes et al, 2011;Wienhausen et al, 2017), including P. inhibens, and can kill the C-type culture, CCMP3266, at high concentrations (1,000 µM) (Labeeuw et al, 2016;Segev et al, 2016). However, Segev et al (2016) also showed that P. inhibens did not produce IAA at high enough concentrations to kill E. huxleyi CCMP3266 (0.4-10 nM).…”

Future prospects of delignification pretreatments for the lignocellulosic materials to produce second generation bioethanol

“…Algal biomass has the ability to grow under harsh conditions like saline, brackish water, which does not affect any conventional agriculture. 133 The disadvantage attached with the use of algal biomass as a feedstock is its higher cultivation cost as compared with conventional crops because of high energy input. Similarly, harvesting of algae requires high energy input, which is 20% to 30% of the total production cost.…”