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Accompanying Botryococcus Braunii bioRxiv preprint doi: https://doi.org/10.1101/476887; this version posted November 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 The ‘zoo’ accompanying Botryococcus braunii: 2 Unraveling the fundamentals of algae-bacteria biocoenosis 3 4 Running title: Fundamentals of algae-bacteria biocoenosis 5 6 Olga Blifernez-Klassen1,2, Viktor Klassen1,2, Daniel Wibberg2, Swapnil Chaudhari1,2, 7 Christian Henke2,3, Anika Winkler2, Arwa Al-Dilaimi2, Oliver Rupp4, Jochen Blom4, 8 Alexander Goesmann4, Alexander Sczyrba2,3, Andrea Bräutigam2,5, Jörn Kalinowski2, 9 Olaf Kruse1,2* 10 11 1Algae Biotechnology and Bioenergy, Faculty of Biology, Bielefeld University, 12 Universitätsstrasse 27, 33615 Bielefeld, Germany 13 2Center for Biotechnology (CeBiTec), Bielefeld University, Universitätsstrasse 27, 33615 14 Bielefeld, Germany 15 3Computational Metagenomics, Faculty of Technology, Bielefeld University, 16 Universitätsstrasse 25, 33615 Bielefeld, Germany 17 4Bioinformatics and Systems Biology, Justus-Liebig-University, Heinrich-Buff-Ring 58, 18 35392 Gießen, Germany 19 5Computational Biology, Faculty of Biology, Bielefeld University, Universitätsstrasse 27, 20 33615 Bielefeld, Germany 21 22 *Address correspondence to: Olaf Kruse, Algae Biotechnology and Bioenergy, Faculty of 23 Biology, Center for Biotechnology (CeBiTec), Bielefeld University, Universitätsstrasse 27, 24 33615 Bielefeld, Germany; phone: +49 521 106-12258; email: [email protected] 25 26 Competing interests 27 The authors declare that they have no competing interests. 28 This work was supported by the European Union Seventh Framework Programme (FP7/2007- 29 2013) under grant agreement 311956 and by the BMBF-funded project “Bielefeld-Gießen 30 Center for Microbial Bioinformatics” – BiGi (grant 031A533). bioRxiv preprint doi: https://doi.org/10.1101/476887; this version posted November 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Fundamentals of algae-bacteria biocoenosis 31 Abstract 32 The interactions between microalgae and bacteria represent a fundamental ecological 33 relationship within aquatic environments, by controlling nutrient cycling and biomass 34 production at the food web base. However, the extent of these interactions and their metabolic 35 significance are poorly understood. To elucidate the complexity of microalga-bacteria 36 interactions, Botryococcus braunii consortia were chosen as a suitable model system with an 37 organic carbon-rich phycosphere. Here we present a comparative metagenome analysis in 38 conjunction with physiological data that allow a deep insight into the community relationship. 39 The reconstruction of ten high-quality draft and two full genomes of the abundant associates 40 clarify consortia’s basic functional characteristics based on the bacterial genetic repertoire. 41 Implying a strong mutualistic algae-bacteria relationship, most abundant members of the 42 Botryococcus phycosphere belong to a distinct niche of B-vitamin auxotrophs, essentially 43 depending on the microalga to provide these important cofactors. This high dependency 44 allows the microalga to effectively control its own phycosphere and impacts the bacteria- 45 bacteria interactions within the consortium. Overall, our results provide highly valuable 46 insights into the fundamentals of microbial ecology where metabolic networks cross species 47 boundaries and define complex interactions. The knowledge of these interactions could enable 48 the design of functional synthetic ecosystems consisting of photosynthetic and heterotrophic 49 microorganisms. 50 51 52 53 54 55 56 2 bioRxiv preprint doi: https://doi.org/10.1101/476887; this version posted November 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Fundamentals of algae-bacteria biocoenosis 57 Introduction 58 Microalgae are the dominant primary producers and the base of the food web within 59 aquatic ecosystems and sustain in the natural environment in close relationship with multiple 60 associated microorganisms [1, 2]. Algae-bacteria interactions, still poorly understood, are 61 multifaceted and complex, and often take place in the microenvironment of individual algal 62 cells, the phycosphere [2, 3]. The spectrum of ecological interrelations within the specific 63 phycosphere ranges from cooperative to competitive [1], where algae and bacteria ‘live 64 together’ within a framework of symbiosis [4]. The nature of the exchange of micro- and 65 macronutrients, diverse metabolites including complex algal products such as 66 polysaccharides, and infochemicals defines the relationship of the symbiotic partners [5, 6], 67 which span mutualism, commensalism and parasitism [2]. Within a parasitic association, the 68 bacteria are known to adversely affect the algae (e.g. cell wall degradation [7]), while in 69 commensalism the partners can survive independently, with the commensal feeding on algae- 70 provided substrates, but without harming the host [2]. Mutualistic interactions include i.a. the 71 obligate relationships between vitamin-synthesizing bacteria and vitamin-auxotrophic 72 phytoplankton species [8]. Many microalgae cannot synthesize several growth-essential 73 vitamins (like B12 and B1) [8–10] and obtain them through a symbiotic relationship with 74 bacteria in exchange for organic carbon [11]. Not only the microalgae require these vitamins, 75 but also many bacteria have to compete with other organisms for the B-vitamins [12]. 76 However, in microbial environments, where the distinction between host and symbionts is 77 less clear, the identification of the associated partners and the nature of their relationship is 78 challenging. Looking for a suitable model system to elucidate the complex interactions 79 between algae and bacteria, we focussed on the lifestyle of the colony-forming and 80 hydrocarbon producing microalga Botryococcus braunii. This green microalga is known to 81 co-exist with heterotrophic microorganisms [13]. The alga-bacteria consortium may represent 82 an example for an association already existing during the early stages of life development on 3 bioRxiv preprint doi: https://doi.org/10.1101/476887; this version posted November 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Fundamentals of algae-bacteria biocoenosis 83 earth, since it is generally considered that a progenitor of Botryococcus impacted the 84 development of today's oil reserves and coal shale deposits [14]. Nowadays, this cosmopolitan 85 microalga is widely considered of enormous biotechnological importance because of its 86 unique ability to produce and secrete large quantities of aliphatic (C20-C40) hydrocarbons and 87 exo-polysaccharides [15]. Due to the excretion of large quantities of organic carbon into its 88 phycosphere, naturally occurring B. braunii cultures are generally not axenic but are 89 associated with a variety of microorganisms [13]. The interactions between B. braunii and the 90 associated bacteria are not fully understood, but are known to influence the microalgal growth 91 performance and product formation capacity [16]. The associated bacteria may stimulate algal 92 growth and product formation [17] or, conversely restrict algal growth by competing for 93 nutrients, degrading algal exopolysaccharides and hydrocarbons, releasing anti-algal 94 substances, or affecting algal morphology [13, 15]. 95 To understand the complex nature of the unique habitat of a microalgal phycosphere and to 96 unravel the food web between alga and bacteria, we investigated the consortium 97 accompanying the hydrocarbon/carbohydrate-producing green microalga Botryococcus 98 braunii. Two B. braunii races (A and B) were sequenced at different time points (linear and 99 stationary growth) for the analysis and identification of the bacterial key players within 100 communities and their ecological impact on the microalga. 101 102 Materials and Methods 103 Strains, cultivation conditions and growth determination parameters. Liquid, xenic 104 cultures of Botryococcus braunii race A (CCALA778, isolated in Serra da Estrela (Baragem 105 da Erva da Fome) Portugal) and race B (AC761, isolated from Paquemar, Martinique, France) 106 as well as the axenic B. braunii race A strain (SAG30.81, Peru, Dpto.Cuzco, Laguna Huaypo) 107 used for co-cultivation studies. The cultures were phototrophically cultivated under 16:8 light- 108 dark illumination of 350±400 μmol photons m-2 s-1 white light in modified Chu-13 media 4 bioRxiv preprint doi: https://doi.org/10.1101/476887; this version posted November 22, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. Fundamentals of algae-bacteria biocoenosis 109 (without the addition of vitamin and organic carbon source) as described before [18]. Carbon 110 supply and agitation were achieved by bubbling the cultures with moisture pre-saturated 111 carbon dioxide-enriched air (5%, v/v) with a gas flow rate of 0.05 vvm. The axenic strain was 112 regularly checked for contaminations. 113 The bacterial isolates
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