Abstract

Microbial biotechnological processes can be based on single species pure cultures or on multi-species assemblages. While these assemblages can be advantageous by offering more functionalities and more resilience to changing environmental conditions, they can be unpredictable and difficult to control under synthetically engineered growth conditions. To overcome the unpredictable nature of these microbial assemblages, the generation of stable mutualistic systems through synthetic ecology approaches may provide novel solutions for understanding microbial interactions in these environments. Here we establish a stable association between two evolutionarily unrelated, but biotechnologically complementary species isolated from winery wastewater; a strain of the yeast Saccharomyces cerevisiae and microalga, Chlorella sorokiniana. Yeast and microalgae were able to form obligate (interdependent) and non-obligate (facultative) mutualisms under engineered batch co-culture growth conditions. Obligate mutualism was maintained through the reciprocal exchange of carbon and nitrogen where the yeast ferments mannose to produce carbon dioxide for use by the microalga; and the microalga provides the yeast with nitrogen by metabolizing nitrite to ammonium. The effect of temperature and pH on the establishment of these mutualisms was evaluated and pH was found to be a key determinant for mutualism formation under obligatory conditions. Moreover, the combinations of the two species under non-obligatory growth conditions led to improvement in growth rate and biomass production when compared to single species cultures grown under the same conditions. Such engineered mutualisms are the first step in developing stable multi-species assemblages, while providing a system to generate novel insight into the evolution of mutualistic interactions between phylogenetically distant microorganisms.

Highlights

  • IntroductionPhotosynthetic microalgae are considered the most efficient producers of biomass for the production of biofuels (bioethanol, biohydrogen, biodiesel, and biogas) and bio-products (animal feeds, omega fatty acids, and carotenoids) (John et al, 2011; Jones and Mayfield, 2012; Borowitzka and Moheimani, 2013)

  • Photosynthetic microalgae are considered the most efficient producers of biomass for the production of biofuels and bio-products (John et al, 2011; Jones and Mayfield, 2012; Borowitzka and Moheimani, 2013)

  • We suggest that multi-species assemblages comprising yeast and microalgae in mutualistic associations might offer increased stability and improved bioremediation efficiency under these variable conditions.Yeasts are attractive candidates for winery wastewater bioremediation as they are readily able to break down the sugars and organic acids which dominate these environments and serve to decrease the chemical oxygen demand (COD) in numerous wastewasters (Malandra et al, 2003; Gharsallah, 2008; Bezuneh, 2016; Wang et al, 2018)

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Summary

Introduction

Photosynthetic microalgae are considered the most efficient producers of biomass for the production of biofuels (bioethanol, biohydrogen, biodiesel, and biogas) and bio-products (animal feeds, omega fatty acids, and carotenoids) (John et al, 2011; Jones and Mayfield, 2012; Borowitzka and Moheimani, 2013). Most microalgae-based processes have not delivered as expected due to a lack of cost-effective technologies for the production of algal biomass at an industrial scale This is due in part to the use of single species, monoculture systems, which work well in laboratory settings but present numerous challenges when up-scaled. Synthetic microbial ecology offers a solution to this problem as multi-species assemblages comprised of microorganisms with complementary metabolic capabilities are generally more robust in the face of environmental change than their monoculture counterparts (Brenner et al, 2008) These artificial assemblages can be designed to incorporate key design elements such as species specific selection and engineered symbiosis; which can serve to improve processes such as wastewater treatment and biofuel production (Lee, 2001; Kazamia et al, 2014). These artificial microbial communities can often perform more complex tasks and the network of interactions between microorganisms results in more stable and robust ecosystems (Brenner et al, 2008; de-Bashan et al, 2016)

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