Department of Biological Sciences, California State University, San Luis Obispo, California, USA.
Department of Microbiology and Immunology, Loyola University Chicago, Maywood, Illinois, USA.
Appl Environ Microbiol. 2024 Jun 18;90(6):e0032824. doi: 10.1128/aem.00328-24. Epub 2024 May 7.
Cells of colonize the light organ of , providing the squid bioluminescence in exchange for nutrients and protection. The bacteria encounter DNA-rich mucus throughout their transition to a symbiotic lifestyle, leading us to hypothesize a role for nuclease activity in the colonization process. In support of this, we detected abundant extracellular nuclease activity in growing cells of . To discover the gene(s) responsible for this activity, we screened a transposon mutant library for nuclease-deficient strains. Interestingly, only one strain, whose transposon insertion mapped to nuclease gene , showed a complete loss of nuclease activity in our screens. A database search revealed that is homologous to the nuclease-encoding gene in . However, strains lacking eventually revealed slight nuclease activity on plates upon prolonged incubation. This led us to hypothesize that a second secreted nuclease, identified through a database search as , a homolog of , might be responsible for the residual nuclease activity. Here, we show that Xds and/or Dns are involved in essential aspects of biology, including natural transformation, aggregation, and phosphate scavenging. Furthermore, strains lacking either nuclease were outcompeted by the wild type for squid colonization. Understanding the specific role of nuclease activity in the squid colonization process represents an intriguing area of future research.IMPORTANCEFrom soil and water to host-associated secretions such as mucus, environments that bacteria inhabit are awash in DNA. Extracellular DNA (eDNA) is a nutritious resource that microbes dedicate significant energy to exploit. Calcium binds eDNA to promote cell-cell aggregation and horizontal gene transfer. eDNA hydrolysis impacts the construction of and dispersal from biofilms. Strategies in which pathogens use nucleases to avoid phagocytosis or disseminate by degrading host secretions are well-documented; significantly less is known about nucleases in mutualistic associations. This study describes the role of nucleases in the mutualism between and its squid host . We find that nuclease activity is an important determinant of colonization in , broadening our understanding of how microbes establish and maintain beneficial associations.
细菌定植于鱿鱼的发光器官,为鱿鱼提供生物发光,同时交换营养物质和保护。在向共生生活方式转变的过程中,细菌会遇到富含 DNA 的黏液,这使我们假设核酸酶活性在定植过程中发挥作用。为了支持这一假设,我们在 的生长细胞中检测到丰富的细胞外核酸酶活性。为了发现负责这种活性的基因,我们筛选了转座子突变体文库,以寻找核酸酶缺陷型菌株。有趣的是,只有一个菌株,其转座子插入位于核酸酶基因 处,在我们的筛选中完全丧失了核酸酶活性。数据库搜索显示, 与核酸酶编码基因 在 中同源。然而,缺失 的 菌株在长时间孵育后在平板上显示出轻微的核酸酶活性。这使我们假设第二种分泌型核酸酶,通过数据库搜索鉴定为 ,是 的同源物,可能负责剩余的核酸酶活性。在这里,我们表明 Xds 和/或 Dns 参与了 生物学的重要方面,包括自然转化、聚集和磷酸盐的摄取。此外,缺乏任何一种核酸酶的菌株在与鱿鱼定植的竞争中被野生型菌株所淘汰。了解核酸酶活性在鱿鱼定植过程中的具体作用是未来研究的一个有趣领域。
重要性
从土壤和水到宿主相关分泌物(如黏液),细菌栖息的环境中充斥着 DNA。细胞外 DNA(eDNA)是一种有营养的资源,微生物会投入大量的能量来利用它。钙结合 eDNA 以促进细胞间的聚集和水平基因转移。eDNA 水解会影响生物膜的构建和扩散。病原体利用核酸酶逃避吞噬或通过降解宿主分泌物传播的策略已得到充分证实;在互利共生关系中,核酸酶的作用则知之甚少。本研究描述了核酸酶在 和其鱿鱼宿主之间的共生关系中的作用。我们发现核酸酶活性是 定植的重要决定因素,这拓宽了我们对微生物如何建立和维持有益联系的理解。