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.
Highlights
Small signaling molecules are important components of interspecies interactions, and have been shown to play a role in multicellularity, settlement, and pathogenesis (Joint et al, 2002; Manefield et al, 2002; Matsuo et al, 2005; Schaefer et al, 2008)
We found homologs of some bacterial indole-3-acetic acid (IAA) biosynthesis genes in algae (Supplementary Table 2), suggesting that alternate pathways for IAA biosynthesis to those found in plants might be present
IAA has been identified from a variety of photosynthetic organisms, including cyanobacteria (Sergeeva et al, 2002; Ahmed et al, 2010; Hussain et al, 2010), chlorophytes (Sztein et al, 2000; Mazur et al, 2001; Jirásková et al, 2009; Stirk et al, 2013), as well as some rhodophytes and brown algae (Le Bail et al, 2010; Mikami et al, 2015), but to our knowledge, this is the first time auxins have been identified from an axenic haptophyte culture
Summary
Small signaling molecules are important components of interspecies interactions, and have been shown to play a role in multicellularity, settlement, and pathogenesis (Joint et al, 2002; Manefield et al, 2002; Matsuo et al, 2005; Schaefer et al, 2008) While these interactions occur at the cell-to-cell interface, they can have large-scale effects at the community and ecosystem levels (Charlson et al, 1987; Vardi et al, 2009; Cooper and Smith, 2015). Current research indicates that signaling molecules are important components of interkingdom communication in bacterial-host systems (Hughes and Sperandio, 2008) One such group of small molecules, which is well-studied in plants, is the phytohormone indole-3-acetic acid (IAA). IAA has commercial use and is frequently sprayed over agricultural fields to increase crop yields (Sudha et al, 2012)
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