Diatom modulation of select bacteria through use of two unique secondary metabolites

Abstract

Unicellular eukaryotic phytoplankton, such as diatoms, rely on microbial communities for survival despite lacking specialized compartments to house microbiomes (e.g., animal gut). Microbial communities have been widely shown to benefit from diatom excretions that accumulate within the microenvironment surrounding phytoplankton cells, known as the phycosphere. However, mechanisms that enable diatoms and other unicellular eukaryotes to nurture specific microbiomes by fostering beneficial bacteria and repelling harmful ones are mostly unknown. We hypothesized that diatom exudates may tune microbial communities and employed an integrated multiomics approach using the ubiquitous diatom Asterionellopsis glacialis to reveal how it modulates its naturally associated bacteria. We show that A. glacialis reprograms its transcriptional and metabolic profiles in response to bacteria to secrete a suite of central metabolites and two unusual secondary metabolites, rosmarinic acid and azelaic acid. While central metabolites are utilized by potential bacterial symbionts and opportunists alike, rosmarinic acid promotes attachment of beneficial bacteria to the diatom and simultaneously suppresses the attachment of opportunists. Similarly, azelaic acid enhances growth of beneficial bacteria while simultaneously inhibiting growth of opportunistic ones. We further show that the bacterial response to azelaic acid is numerically rare but globally distributed in the world’s oceans and taxonomically restricted to a handful of bacterial genera. Our results demonstrate the innate ability of an important unicellular eukaryotic group to modulate select bacteria in their microbial consortia, similar to higher eukaryotes, using unique secondary metabolites that regulate bacterial growth and behavior inversely across different bacterial populations.

Surface Topography, Bacterial Carrying Capacity, and the Prospect of Microbiome Manipulation in the Sea Anemone Coral Model Aiptasia

“…First off, our results show that all transplanted animals harbor a significantly different active bacterial community when compared to control anemones with the general notion that inoculated Aiptasia resemble each other more than control animals (Figure 4 and Supplementary Table 5). This is not highly surprising given that formation of an established microbial community may take time and likely goes through processes of inter-bacterial communication, host-bacterial communication, and winnowing, all of which presumably affect microbiome composition (Franzenburg et al, 2013a;Bernasconi et al, 2019;Shibl et al, 2020). As such, microbial consortia associated with Aiptasia after microbiome transplantation might represent a mix of specific bacteria administered with the inocula and opportunistic, environmentally present bacteria (e.g., resistant bacteria that survived the antibiotic treatment and were attached to the wells of the rearing plate), in particular copiotrophs.…”

Mechanisms Driving Genome Reduction of a NovelRoseobacterLineage Showing Vitamin B12Auxotrophy

“…They usually benefit from the fixed carbon or other excretions released by phytoplankton and, in return, produce secondary metabolites (e.g. vitamins, indole-3-acetic acid) to promote phytoplankton growth (15, 67, 68). These interactions likely occur in microzones immediately surrounding phytoplankton cells, which may create gene flow barriers and facilitate population differentiation of associated roseobacters (69).…”

Scaling down the microbial loop: data-driven modelling of growth interactions in a diatom-bacterium co-culture

“…Also, the composition of the diatom-associated bacterial community has been shown to play a role in regulating the physiological status of this biological system (Behringer et al 2018;Moejes et al 2017;Rooney-Varga et al 2005) and to be the subject of specific regulatory rules. In a recent work, Shibl et al (2020) showed that diatom exudates might tune microbial communities and select specific bacteria of their associated consortium. This is achieved through the secretion of secondary metabolites that promote the proliferation of selected bacteria and demote others (Shibl et al 2020).…”

“…In a recent work, Shibl et al (2020) showed that diatom exudates might tune microbial communities and select specific bacteria of their associated consortium. This is achieved through the secretion of secondary metabolites that promote the proliferation of selected bacteria and demote others (Shibl et al 2020). Further, Moejes et al (2017) have characterized the microbiome associated with the model pennate diatom Phaeodactylum tricornutum and proposed a network of putative interactions between the diatom and the main bacterial taxa found in the community.…”