Recognition cascade and metabolite transfer in a marine bacteria‐phytoplankton model system

Abstract

The trophic linkage between marine bacteria and phytoplankton in the surface ocean is a key step in the global carbon cycle, with almost half of marine primary production transformed by heterotrophic bacterioplankton within hours to weeks of fixation. Early studies conceptualized this link as the passive addition and removal of organic compounds from a shared seawater reservoir. Here, we analysed transcript and intracellular metabolite patterns in a two-member model system and found that the presence of a heterotrophic bacterium induced a potential recognition cascade in a marine phytoplankton species that parallels better-understood vascular plant response systems. Bacterium Ruegeria pomeroyi DSS-3 triggered differential expression of >80 genes in diatom Thalassiosira pseudonana CCMP1335 that are homologs to those used by plants to recognize external stimuli, including proteins putatively involved in leucine-rich repeat recognition activity, second messenger production and protein kinase cascades. Co-cultured diatoms also downregulated lipid biosynthesis genes and upregulated chitin metabolism genes. From differential expression of bacterial transporter systems, we hypothesize that nine diatom metabolites supported the majority of bacterial growth, among them sulfonates, sugar derivatives and organic nitrogen compounds. Similar recognition responses and metabolic linkages as observed in this model system may influence carbon transformations by ocean plankton.

Identification of Bacterial Genes Expressed During Diatom-Bacteria Interactions Using an in Vivo Expression Technology Approach

“…In this context, we identified six genetic loci, which unfortunately do not allow concluding anything directly in terms of increased catabolism or accelerated energy conservation during the co-culture (col. 15, 19, 24, 149, 205, and 240). However, these results confirmed previous metagenomic and transcriptomic studies in which genes for degradation of organic compounds and an increase in bacterial activity and cell division rates were identified during bacteriaalgae interactions (Poretsky et al, 2010;Smith et al, 2013;Durham et al, 2017).…”

“…In addition, IVET avoids some of the potential next-generation sequencing biases, such as problems associated with highthroughput cDNA generation and high-throughput nucleotide sequencing. Although IVET itself has biases such as being rather qualitative than quantitative and that the required absolute length of insert DNA in the IVET library or low level of expression from some promoters might exclude certain genes or groups of genes, the herein applied approach complements transcriptomics work of others (Durham et al, , 2017 and our own proteomics work (Stahl and Ullrich, 2016). Others had shown previously that IVET can be used to identify novel genes important for the respective analyzed interactions (Rediers et al, 2005;Dudley, 2008).…”

“…Although it is widely accepted that promoters drive the expression of directly downstream located genes, our study did not detect the expression of those genes. However, finding active promoters for some genes, which code for proteins previously detected by a proteomics approach (Stahl and Ullrich, 2016) as well as finding gene homologs found by transcriptomics studies of others (Durham et al, 2017) are strong hints for a successful screening approach. In the next paragraphs, the possible ecological roles and importance of the identified genes are discussed.…”

“…Gene expression analysis has identified an increase of transcripts involved in DOC uptake when bacteria interact with algae, e.g., transport systems for amino acid, carboxylic acids, carbohydrates (Poretsky et al, 2005(Poretsky et al, , 2010Rinta-Kanto et al, 2012;Teeling et al, 2012;Durham et al, 2017). In the current study, several promoters driving the expression of genes involved in the uptake of organic-mainly nitrogen-containing-compounds were identified.…”

“…Initially mediated by either simple collision events or diverse chemical reactions, diatom-bacteria interactions initialize, or reinforce these processes by formation of extra-cellular polysaccharides affecting the stickiness and hence size of aggregates Logan et al, 1995;Passow, 2002). In the last decade, considerable progress has been made in understanding algae-bacteria interactions at both, the ecological as well as the cellular and molecular levels (Wang et al, 2014;Amin et al, 2015;Durham et al, 2015Durham et al, , 2017Needham et al, 2017;van Tol et al, 2017). In this way, different types of interactions were discovered, which were either microbial population driven or dictated by individual bacterial organisms.…”