Microalgae show a range of responses to exometabolites of foreign species

Natalia G Apostolopoulou; Evangelia Smeti; Marta Lamorgese; Ioanna Varkitzi; Phillip Whitfield; Clement Regnault; Sofie Spatharis

doi:10.1016/j.algal.2021.102627

Microalgae show a range of responses to exometabolites of foreign species

Algal Res. 2022 Mar:62:None. doi: 10.1016/j.algal.2021.102627.

Authors

Natalia G Apostolopoulou^{1

2}, Evangelia Smeti³, Marta Lamorgese², Ioanna Varkitzi⁴, Phillip Whitfield⁵, Clement Regnault⁵, Sofie Spatharis^{2

6}

Affiliations

¹ Department of Ecology and Systematics, National and Kapodistrian University of Athens, 10679, Greece.
² School of Life Sciences, University of Glasgow, G12 8QQ, UK.
³ Institute of Marine Biological Resources and Inland Waters, HCMR Hellenic Centre for Marine Research, PO Box 713, Anavyssos 19013, Greece.
⁴ Institute of Oceanography, HCMR Hellenic Centre for Marine Research, PO Box 713, Anavyssos 19013, Greece.
⁵ Glasgow Polyomics, University of Glasgow, G61 1BD, UK.
⁶ Institute of Biodiversity, Animal Health & Comparative Medicine, University of Glasgow, G12 8QQ, UK.

Abstract

Studies on microalgae interspecific interactions have so far focused either on nutrient competition or allelopathic effects due to excreted substances from Harmful Algal Bloom (HAB) species. Evidence from plants, bacteria and specific microalgae groups, point to a range of responses mediated by sensing or direct chemical impact of exometabolites from foreign species. Such processes remain under-investigated, especially in non-HAB microalgae, despite the importance of such knowledge in ecology and industrial applications. Here, we study the directional effect of exometabolites of 4 "foreign" species Heterosigma akashiwo, Phaeocystis sp., Tetraselmis sp. and Thalassiosira sp. to each of three "target" species across a total of 12 treatments. We disentangle these effects from nutrient competition by adding cell free medium of each "foreign" species into our treatment cultures. We measured the biomass response, to the foreign exometabolites, as cell number and photosynthetic biomass (Chla), whereas nutrient use was measured as residual phosphorus (PO₄) and intracellular phosphorus (P). Exometabolites from filtrate of foreign species were putatively annotated by untargeted metabolomics analysis and were discussed in association to observed responses of target species. Among others, these metabolites included L-histidinal, Tiliacorine and dimethylsulfoniopropionate (DMSP). Our findings show that species show a range of responses with the most common being biomass suppression, and less frequent biomass enhancement and intracellular P storage. Filtrate from the green microalgae Tetraselmis caused the most pronounced negative effects suggesting that non-HAB species can also cause negative chemical interference. A candidate metabolite inducing this response is L-histidinal which was measured in high abundance uniquely in Tetraselmis and its L-histidine form derived from bacteria was previously confirmed as a microalgal algicidal. H. akashiwo also induced biomass suppression on other microalgae and a candidate metabolite for this response is Tiliacorine, a plant-derived alkaloid with confirmed cytotoxic activity.

Keywords: Exometabolites; Intracellular phosphorus; L-histidinal; Luxurious phosphorus uptake; Microalgae; Tiliacorine.