Exploring the functional and genomic features of Cellulophaga lytica NFXS1, a zeaxanthin and lytic enzyme-producing marine bacterium that promotes microalgae growth

Constança D.F. Bertrand , Rodrigo Martins , Francisco Quintas-Nunes , Pedro Reynolds-Brandão , Maria T. Barreto Crespo , Francisco X. Nascimento
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Abstract

Beneficial microalgae-bacteria interactions mediate important marine ecological processes and present potential for exploitation in the industrial production of microalgae. Members of the bacterial genus Cellulophaga are known for their ability to interact with several marine organisms, including microalgae, however, not much is understood about their properties. In this work we present the detailed characterization of the marine bacterium, Cellulophaga lytica NFXS1, including its ability to synthesize valuable compounds such as zeaxanthin, its ability to modulate the growth and productivity of two relevant marine microalgae, Nannochloropsis oceanica and Phaeodactylum tricornutum, and the analysis of its complete genome sequence. The obtained results showed that C. lytica NFXS1 used several complex carbohydrates, indicating strong lytic enzymatic activities. Additionally, co-cultivation studies revealed that C. lytica NFXS1 colonized the microalgae phycosphere, catabolized microalgae exudates, promoted the growth of microalgae, and increased fucoxanthin productivity in P. tricornutum. Genomic analysis revealed the basis for the microalgae growth-promoting activities of strain NFXS1, which are mostly mediated by gliding motility, biofilm formation, biosynthesis of phytohormones (auxins, cytokinins), polyamine biosynthesis, and resistance to oxidative stress induced by zeaxanthin production and ROS detoxifying enzymes. A vast array of genes encoding glycosyl hydrolases and pectate lyase family enzymes were also found in the NFXS1 chromosome. Overall, these findings brought new information regarding the properties of C. lytica NFXS1, which can be used as a model organism to study microalgae-bacteria interactions and is a strong candidate for the development of a wide range of marine biotechnological solutions.

探索促进微藻类生长的玉米黄质和裂解酶海洋细菌 Cellulophaga lytica NFXS1 的功能和基因组特征
有益的微藻-细菌相互作用介导着重要的海洋生态过程,并为微藻的工业化生产提供了开发潜力。众所周知,嗜纤维细菌属的成员能够与包括微藻类在内的多种海洋生物发生相互作用,但人们对它们的特性了解不多。在这项工作中,我们详细介绍了海洋细菌 Cellulophaga lytica NFXS1 的特性,包括其合成玉米黄质等有价值化合物的能力、调节两种相关海洋微藻 Nannochloropsis oceanica 和 Phaeodactylum tricornutum 的生长和生产力的能力,以及对其完整基因组序列的分析。研究结果表明,C. lytica NFXS1 使用了多种复杂的碳水化合物,表明其具有很强的溶解酶活性。此外,共培养研究表明,C. lytica NFXS1 能定植于微藻类植物圈,分解微藻类渗出物,促进微藻类的生长,并提高三尖杉属褐藻黄质的产量。基因组分析揭示了菌株 NFXS1 促进微藻生长活性的基础,这些活性主要由滑行运动、生物膜形成、植物激素(辅助素、细胞分裂素)的生物合成、多胺生物合成以及由玉米黄质生产和 ROS 解毒酶诱导的抗氧化压力介导。在 NFXS1 染色体中还发现了大量编码糖基水解酶和酪酸酶家族酶的基因。总之,这些发现为研究莱卡藻 NFXS1 的特性提供了新的信息。莱卡藻 NFXS1 可作为研究微藻与细菌相互作用的模式生物,也是开发多种海洋生物技术解决方案的有力候选者。
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