The ability of Phaeobacter inhibens to produce tropodithietic acid influences the community dynamics of a microalgal microbiome

Abstract

Microbial secondary metabolites facilitate microbial interactions and are crucial for understanding the complexity of microbial community dynamics. The purpose of the present study was to determine how a secondary metabolite producing marine bacteria or its metabolite deficient mutant affected the microbiome of the marine microalgae Tetraselmis suecica during a 70 day long co-evolution experiment. Using 16S rRNA gene amplicon sequencing, we found that neither the tropodithietic acid (TDA)-producing Phaeobacter inhibens wildtype nor the TDA-deficient mutant had major impacts on the community composition. However, a subset of strains, displayed temporally different relative abundance trajectories depending on the presence of P. inhibens. In particular, a Winogradskyella strain displayed temporal higher relative abundance when the TDA-producing wildtype was present. Numbers of the TDA-producing wildtype were reduced significantly more than those of the mutant over time indicating that TDA production was not an advantage. In communities without the P. inhibens wildtype strain, an indigenous population of Phaeobacter increased over time, indicating that indigenous Phaeobacter populations cannot co-exist with the TDA-producing wildtype. Despite that TDA was not detected chemically, we detected transcripts of the tdaC gene indicating that TDA could be produced in the microbial community associated with the algae. Our work highlights the importance of deciphering longitudinal strain dynamics when addressing the ecological effect of secondary metabolites in a relevant natural community.

The potential to produce tropodithietic acid by Phaeobacter inhibens affects the assembly of microbial biofilm communities in natural seawater

“…The positive association between the P. inhibens when it is capable of producing TDA and the Flavobacteriales including Winogradskyella spp. has been observed in previous studies describing different marine systems such as non-axenic algal and oyster microbiomes 42,43 . The fact that several members of the Bacteroidetes are motile by gliding 39 and that the TDA-producing Phaeobacter species most frequently have been isolated from harbor surfaces 20,44 , suggests that they could compete for surface colonization space in nature.…”

Understanding the biosynthesis, metabolic regulation, and anti-phytopathogen activity of 3,7-dihydroxytropolone inPseudomonasspp

“…The tropolone chemophore is found in a variety of bioactive specialised metabolites 22,23 . These molecules have broad ecological relevance 60,61 and medicinal promise, where some synthetic derivatives are under investigation as lead compounds for multiple diseases [62][63][64][65] . Here, we have demonstrated that the tropolone (tpo) BGC in Pseudomonas sp.…”

“…Future efforts should focus on understanding the function of tropolones in natural plant and soil colonisation conditions, as well as the interplay with other BGCs and proteins encoded in tropolone producers 19,69 (Figure 2). For example, recent work by Gram and colleagues has highlighted the impact of tropodithietic acid on Phaeobacter species and associated microbial communities 60,61 .…”

Impact of host species on assembly, composition, and functional profiles of phycosphere microbiomes

“…Rhodobacteraceae and Flavobacteriaceae are families that are commonly associated with phytoplankton blooms and microalgal microbiomes (2, 37, 86). Rhodobacteraceae have been found in association with several species of diatoms, including Phaeodactylum and Thalassiosira (28, 29, 87).…”

“…Microalgae are fundamental to aquatic ecosystems and are the main primary producers of the oceans. Therefore, microalgae have become popular model systems in the field of microbial ecology allowing studies of host-microbiome interactions (1)(2)(3)(4)(5). Also, they are important components of many industrial processes, for instance as live feed in aquaculture (6)(7)(8)(9) and as cell factories in the production of biofuels, nutraceuticals, and natural pigments (10,11).…”