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Sharing Vitamin B12 between Bacteria and Microalgae Does Not Systematically Occur: Case Study of the Haptophyte Tisochrysis lutea

ABSTRACT: Haptophyte microalgae are key contributors to microbial communities in many environments. It has been proposed recently that members of this group would be virtually all dependent on vitamin B12 (cobalamin), an enzymatic cofactor produced only by some bacteria and archaea. Here, we examined the processes of vitamin B12 acquisition by haptophytes. We tested whether co-cultivating the model species Tisochrysis lutea with B12-producing bacteria in vitamin-deprived conditions would allow the microalga to overcome B12 deprivation. While T. lutea can grow by scavenging vitamin B12 from bacterial extracts, co-culture experiments showed that the algae did not receive B12 from its associated bacteria, despite bacteria/algae ratios supposedly being sufficient to allow enough vitamin production. Since other studies reported mutualistic algae–bacteria interactions for cobalamin, these results question the specificity of such associations. Finally, cultivating T. lutea with a complex bacterial consortium in the absence of the vitamin partially rescued its growth, highlighting the importance of microbial interactions and diversity. This work suggests that direct sharing of vitamin B12 is specific to each species pair and that algae in complex natural communities can acquire it indirectly by other mechanisms (e.g., after bacterial lysis).

SUBMITTER: Nef C

PROVIDER: S-EPMC9323062 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Dynamic xanthophyll cycle (XC) related non-photochemical quenching (NPQd, also called qE) is present in most phototrophs. It allows dissipating excess light energy under adverse growing conditions. Generally, NPQd rapidly reverses for photosynthesis to resume when light intensity decreases back toward optimal intensity. Under certain environmental conditions and/or in some species, NPQ can be strongly sustained (NPQs showing hours-to-days relaxation kinetics). Tisochrysis lutea is a South Pacific haptophyte phytoplankton with a strong potential for aquaculture and biotechnology applications. It was previously reported to show a surprisingly low NPQd capacity while synthesizing large amounts of diatoxanthin (Dt), a pigment involved in the XC. In order to better understand this paradox, we investigated the characteristics of NPQ in T. lutea under various growth conditions of light and nutrient availability (different photoperiods, low and high light, nutrient starvations). We found a strong NPQs, unmeasurable with usual fluorometry protocols. Along with confirming the involvement of Dt in both NPQd and NPQs (by using the dithiothreitol inhibitor), we highlighted a strong relationship between Dt and the maximum quantum yield of photochemistry (Fv/Fm) across growing conditions and during relaxation experiments in darkness. It suggests that changes in Fv/Fm, usually attributed to the 'photoinhibitory' quenching (qI), are simultaneously largely impacted by photoprotective NPQ. The overlap of xanthophyll pigments-related photoprotective NPQ with several other mechanisms involved in the cell response (Photosystem II photoinactivation, changes in pigments composition, and detoxification by antioxidants) to energy unbalance is further discussed. Our findings question both how widespread NPQs is in the global ocean, particularly in nutrient starved environments (oligotrophic waters) and situations (post-bloom), and the use of adapted active fluorescence protocols (i.e. with extended NPQ relaxation period prior to measurement).

Project description:The production of polyunsaturated fatty acids (PUFA) in Tisochrysis lutea was studied using the gradual incorporation of a 13C-enriched isotopic marker, 13CO2, for 24 h during the exponential growth of the algae. The 13C enrichment of eleven fatty acids was followed to understand the synthetic pathways the most likely to form the essential polyunsaturated fatty acids 20:5n-3 (EPA) and 22:6n-3 (DHA) in T. lutea. The fatty acids 16:0, 18:1n-9 + 18:3n-3, 18:2n-6, and 22:5n-6 were the most enriched in 13C. On the contrary, 18:4n-3 and 18:5n-3 were the least enriched in 13C after long chain polyunsaturated fatty acids such as 20:5n-3 or 22:5n-3. The algae appeared to use different routes in parallel to form its polyunsaturated fatty acids. The use of the PKS pathway was hypothesized for polyunsaturated fatty acids with n-6 configuration (such as 22:5n-6) but might also exist for n-3 PUFA (especially 20:5n-3). With regard to the conventional n-3 PUFA pathway, Δ6 desaturation of 18:3n-3 appeared to be the most limiting step for T. lutea, "stopping" at the synthesis of 18:4n-3 and 18:5n-3. These two fatty acids were hypothesized to not undergo any further reaction of elongation and desaturation after being formed and were therefore considered "end-products". To circumvent this limiting synthetic route, Tisochrysis lutea seemed to have developed an alternative route via Δ8 desaturation to produce longer chain fatty acids such as 20:5n-3 and 22:5n-3. 22:6n-3 presented a lower enrichment and appeared to be produced by a combination of different pathways: the conventional n-3 PUFA pathway by desaturation of 22:5n-3, the alternative route of ω-3 desaturase using 22:5n-6 as precursor, and possibly the PKS pathway. In this study, PKS synthesis looked particularly effective for producing long chain polyunsaturated fatty acids. The rate of enrichment of these compounds hypothetically synthesized by PKS is remarkably fast, making undetectable the 13C incorporation into their precursors. Finally, we identified a protein cluster gathering PKS sequences of proteins that are hypothesized allowing n-3 PUFA synthesis.

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Sharing Vitamin B12 between Bacteria and Microalgae Does Not Systematically Occur: Case Study of the Haptophyte Tisochrysis lutea

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