Pelagibaca bermudensis promotes biofuel competence of Tetraselmis striata in a broad range of abiotic stressors: dynamics of quorum-sensing precursors and strategic improvement in lipid productivity

Abstract

BackgroundAmelioration of biofuel feedstock of microalgae using sustainable means through synthetic ecology is a promising strategy. The co-cultivation model (Tetraselmis striata and Pelagibaca bermudensis) was evaluated for the robust biofuel production under varying stressors as well as with the selected two-stage cultivation modes. In addition, the role of metabolic exudates including the quorum-sensing precursors was assessed.ResultsThe co-cultivation model innovated in this study supported the biomass production of T. striata in a saline/marine medium at a broad range of pH, salinity, and temperature/light conditions, as well as nutrient limitation with a growth promotion of 1.2–3.6-fold. Hence, this developed model could contribute to abiotic stress mitigation of T. striata. The quorum-sensing precursor dynamics of the growth promoting bacteria P. bermudensis exhibited unique pattern under varying stressors as revealed through targeted metabolomics (using liquid chromatography–mass spectrometry, LC–MS). P. bermudensis and its metabolic exudates mutually promoted the growth of T. striata, which elevated the lipid productivity. Interestingly, hydroxy alkyl quinolones independently showed growth inhibition of T. striata on elevated concentration. Among two-stage cultivation modes (low pH, elevated salinity, and nitrate limitation), specifically, nitrate limitation induced a 1.5 times higher lipid content (30–31%) than control in both axenic and co-cultivated conditions.ConclusionPelagibaca bermudensis is established as a potential growth promoting native phycospheric bacteria for robust biomass generation of T. striata in varying environment, and two-stage cultivation using nitrate limitation strategically maximized the biofuel precursors for both axenic and co-cultivation conditions (T and T-PB, respectively). Optimum metabolic exudate of P. bermudensis which act as a growth substrate to T. striata surpasses the antagonistic effect of excessive hydroxy alkyl quinolones [HHQ, 4-hydroxy-2-alkylquinolines and PQS (pseudomonas quorum signal), 2-heptyl-3-hydroxy-4(1H)-quinolone].Electronic supplementary materialThe online version of this article (10.1186/s13068-018-1097-9) contains supplementary material, which is available to authorized users.

Bromination of alkyl quinolones by Microbulbifer sp. HZ11, a marine Gammaproteobacterium, modulates their antibacterial activity

“…Aside from its own genetic potential to synthesize AQs, it is well conceivable that strain HZ11 is exposed to exogenous AQ type metabolites in its natural habitats. This can be concluded from various reports on AQs and AQNOs originating from marine bacteria naturally occurring on biological surfaces or marine organic particles (marine snow; Bultel-Poncé et al, 1999;Long et al, 2003;Patidar et al, 2018). In such a scenario, the bromination of AQs would grant Microbulbifer sp.…”

“…This enzyme is encoded within the biosynthetic gene cluster, providing additional evidence for at least a low-level gene expression. Thus, strain HZ11 is one of only three organisms identified with the metabolic potential to synthesize PQS (Pesci et al, 1999;Patidar et al, 2018).…”

“…In particular, the complex ecosystems of biotic surfaces appear to promote the diversification of secondary metabolites to mediate dynamic inter-species and inter-domain interactions (Penesyan et al, 2010;Giordano et al, 2015). Among the variety of microbial secondary metabolites, 2-alkyl-1(H)-quinolin-4-ones [hereafter referred to as alkyl quinolones (AQs)] have been found to be produced by a number of marine representatives of the Pseudomonas, Alteromonas and Pseudoalteromonas clades as well as the Alphaproteobacterium Pelagibaca bermudensis (Wratten et al, 1977;Debitus et al, 1998;Bultel-Poncé et al, 1999;Long et al, 2003;Vynne et al, 2011;Whalen et al, 2015;Harvey et al, 2016;Kim et al, 2016;Patidar et al, 2018).…”

“…AQs have also attracted considerable attention due to their potential to inhibit growth and motility of various bacteria (Reen et al, 2011). A number of reports suggest a complex ecological role of AQ producing bacteria in marine microbial and/or algal communities (Long et al, 2003;Harvey et al, 2016;Patidar et al, 2018). In particular, HHQ and/or PHQ (2-pentyl-1(H)-quinolin-4-one) produced by Pseudomonas sp.…”

“…HHQ and PQS production were also reported for P. bermudensis, a symbiont of the chlorophyte Tetraselmis striata. In spite of the antagonistic effects of the AQs, the influence of the symbiont on the growth rate of T. striata was reported to be beneficial under certain stress conditions (Patidar et al, 2018). Besides 2-nonyl-and 2-undecyl-1(H)-quinolin-4-ones, 2-nonyl-1-hydroxyquinolin-4-one was isolated from a marine pseudomonad associated with the surface of the sponge Homophymia sp.…”