Frontiers Science Center for Deep Ocean Multispheres and Earth System & College of Marine Life Sciences, Ocean University of Chinagrid.4422.0, Qingdao, China.
Institute of Evolution & Marine Biodiversity, Ocean University of Chinagrid.4422.0, Qingdao, China.
Appl Environ Microbiol. 2022 Dec 13;88(23):e0138922. doi: 10.1128/aem.01389-22. Epub 2022 Nov 21.
Alginate is an important polysaccharide in the ocean that supports the growth of marine microorganisms. Many widespread species possess alginate lyases and can utilize alginate as a carbon source, but the detailed alginate degradation mechanism in remains to be further explored. In this study, we obtained a highly efficient alginate-degrading strain, Vibrio pelagius WXL662, with 11 alginate lyases (VpAly-I to -XI) and further elucidated its molecular mechanism of alginate degradation. Three alginate utilization loci (AUL) were identified in different parts of WXL662's genome, comprising six alginate lyases (VpAly-I, -II, -VIII, -IX, -X, and -XI) and other genes related to alginate degradation. Most of the alginate-degrading genes are strongly induced when alginate is provided as the sole carbon source. Ten alginate lyases (VpAly-I to -X) had been purified and characterized, including six from polysaccharide lyase family 7 (PL7), three from PL17, and one from PL6. These recombinant alginate lyases existing in different cellular locations were active at a wide temperature (10 to 50°C) and pH (4.0 to 9.0) range, with different substrate preferences and diverse degradation products, enabling WXL662 to efficiently utilize alginate in a changing marine environment. Importantly, outer membrane vesicles (OMVs) can act as vectors for alginate lyases (VpAly-II, -V, and -VI) in WXL662. Further investigations of public genomes revealed that most alginate-degrading vibrios possess one AUL instead of previously reported "scattered" system. These results emphasize the specific alginate degradation strategy in Vibrio pelagius WXL662, which can be used as a model strain to study the ecological importance of effective alginate-degrading vibrios in the ocean. Alginate is an important carbon source in the marine environment, and vibrios are major alginate utilizers. Previous studies focused only on the characteristics of individual alginate lyases in vibrios, but few of them discussed the comprehensive alginate-degrading strategy. Here, we depicted the alginate utilization mechanism and its ecological implications of a highly efficient alginate-degrading strain, WXL662, which contained 11 alginate lyases with distinct enzymatic characteristics. Importantly, unlike other vibrios with only one alginate utilization locus (AUL) or the previously reported "scattered" system, three AUL were identified in WXL662. Additionally, the involvement of outer membrane vesicles (OMVs) in the secretion of alginate lyases is proposed for the first time.
海藻酸盐是海洋中一种重要的多糖，它支持海洋微生物的生长。许多广泛存在的物种拥有海藻酸盐裂解酶，可以将海藻酸盐作为碳源加以利用，但海藻酸盐在海洋中的详细降解机制仍有待进一步探索。在本研究中，我们获得了一株高效的海藻酸盐降解菌——海洋弧菌 WXL662，它含有 11 种海藻酸盐裂解酶（VpAly-I 到 -XI），并进一步阐明了其海藻酸盐降解的分子机制。在 WXL662 基因组的不同部位鉴定出了三个海藻酸盐利用基因座（AUL），其中包含六个海藻酸盐裂解酶（VpAly-I、-II、-VIII、-IX、-X 和 -XI）和其他与海藻酸盐降解相关的基因。当提供海藻酸盐作为唯一碳源时，大多数海藻酸盐降解基因被强烈诱导。已经纯化和表征了十个海藻酸盐裂解酶（VpAly-I 到 -X），其中六个来自多糖裂解酶家族 7（PL7），三个来自 PL17，一个来自 PL6。这些存在于不同细胞位置的重组海藻酸盐裂解酶在很宽的温度（10 到 50°C）和 pH（4.0 到 9.0）范围内具有活性，对底物具有不同的偏好，并且具有不同的降解产物，使 WXL662 能够在不断变化的海洋环境中有效利用海藻酸盐。重要的是，外膜囊泡（OMVs）可以作为 WXL662 中海藻酸盐裂解酶（VpAly-II、-V 和 -VI）的载体。对公共基因组的进一步研究表明，大多数海藻酸盐降解弧菌只拥有一个 AUL，而不是之前报道的“分散”系统。这些结果强调了海洋弧菌 WXL662 中特定的海藻酸盐降解策略，它可以作为一个模型菌株，用于研究海洋中有效降解海藻酸盐的弧菌的生态重要性。海藻酸盐是海洋环境中的一种重要碳源，弧菌是主要的海藻酸盐利用者。以前的研究只关注于弧菌中单个海藻酸盐裂解酶的特性，但很少有研究讨论全面的海藻酸盐降解策略。在这里，我们描绘了一株高效的海藻酸盐降解菌 WXL662 的海藻酸盐利用机制及其生态意义，它含有 11 种具有不同酶学特性的海藻酸盐裂解酶。重要的是，与其他只拥有一个海藻酸盐利用基因座（AUL）或之前报道的“分散”系统的弧菌不同，在 WXL662 中鉴定出了三个 AUL。此外，我们首次提出了外膜囊泡（OMVs）在海藻酸盐裂解酶分泌中的参与。
