Bacterial transcriptional response to labile exometabolites from photosynthetic picoeukaryote Micromonas commoda

Abstract

Dissolved primary production released into seawater by marine phytoplankton is a major source of carbon fueling heterotrophic bacterial production in the ocean. The composition of the organic compounds released by healthy phytoplankton is poorly known and difficult to assess with existing chemical methods. Here, expression of transporter and catabolic genes by three model marine bacteria (Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) was used as a biological sensor of metabolites released from the picoeukaryote Micromonas commoda RCC299. Bacterial expression responses indicated that the three species together recognized 38 picoeukaryote metabolites. This was consistent with the Micromonas expression of genes for starch metabolism and synthesis of peptidoglycan-like intermediates. A comparison of the hypothesized Micromonas exometabolite pool with that of the diatom Thalassiosira pseudonana CCMP1335, analyzed previously with the same biological sensor method, indicated that both phytoplankton released organic acids, nucleosides, and amino acids, but differed in polysaccharide and organic nitrogen release. Future ocean conditions are expected to favor picoeukaryotic phytoplankton over larger-celled microphytoplankton. Results from this study suggest that such a shift could alter the substrate pool available to heterotrophic bacterioplankton.

Heterotrophic bacteria trigger transcriptome remodelling in the photosynthetic picoeukaryote Micromonas commoda

“…Another potential mechanism underlying enhanced cell numbers is bacterial release of a growth altering factor as has been observed in studies with other phytoplankton (Amin et al, 2015 ; Seyedsayamdost et al, 2011 ) as well as in land plants (Spaepen & Vanderleyden, 2011 ). The hormone indole‐3‐acetic‐acid (IAA) has been documented to encourage phytoplankton cell division (Amin et al, 2015 ), but none of the bacteria in this study have a complete tryptophan‐dependent IAA biosynthesis pathway (Ferrer‐González et al, 2023 ). While IAA‐based interactions can likely be ruled out, the potential for a growth enhancing metabolite released by the bacteria remains an open question.…”

“…The RNA extraction and sequencing was performed as described in Ferrer‐González et al ( 2023 ). In brief, filters ( n = 4 or 3 per treatment) were individually incubated in TE buffer, SDS (0.6% final concentration) and proteinase K (120 ng μL −1 final concentration), then extracted in equal volumes of acid phenol:chloroform:isoamyl alcohol (25:24:1) and chloroform: isoamyl alcohol (24:1).…”

“…Prior to sequencing, the DNA was processed with the NEBNext rRNA Depletion Kit (E7860; New England Bio Labs, Ipswich, MA), modified to remove M. commoda and bacterial rRNA using a custom pool of 160 oligonucleotide probes (Ferrer‐González et al, 2023 ). The NEBNext Ultra II Directional Kit (E7765) was used for library preparation, which were sequenced at the Georgia Genomics and Bioinformatics Core (Athens, GA, USA) on the NextSeq 2000 platform (SE100; Illumina, San Diego, CA, USA).…”

“…Our previous work established individual co‐cultures between Micromonas commoda and three heterotrophic bacterial taxa: Ruegeria pomeroyi DSS‐3, Stenotrophomonas sp. SKA14 and Polaribacter dokdonensis MED152 (Ferrer‐González et al, 2023 ). Gene expression by the bacteria was the focus of the previous study, using transcription patterns as biological reporters of metabolites released by the phytoplankter.…”

Digital Microbe: A Genome-Informed Data Integration Framework for Collaborative Research on Emerging Model Organisms

“…This meta-analysis captured responses by R. pomeroyi to available substrates under 43 different ecological conditions (Figure 4), including during co-culture growth with phytoplankton (Landa et al 2017; Ferrer-González et al 2023, 2021; Olofsson et al 2022), on defined single or mixed substrates (Bullock et al 2014), and after introduction into a natural phytoplankton bloom (Nowinski and Moran 2021). At the broadest scale, the transporters enabling organic acid uptake (acetate, citrate, fumarate, and 3-hydroxybutyrate) had the highest relative expression across conditions, together accounting for an average of 48%, ranging from 9.7 – 86%, of the transcripts for transporters with confirmed substrates.…”