Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA.
Division of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, Connecticut, USA.
mBio. 2019 Oct 29;10(5):e02376-19. doi: 10.1128/mBio.02376-19.
The importance of defensive symbioses, whereby microbes protect hosts through the production of specific compounds, is becoming increasingly evident. Although defining the partners in these associations has become easier, assigning function to these relationships often presents a significant challenge. Here, we describe a functional role for a bacterial consortium in a female reproductive organ in the Hawaiian bobtail squid, Bacteria from the accessory nidamental gland (ANG) are deposited into the egg jelly coat (JC), where they are hypothesized to play a defensive role during embryogenesis. Eggs treated with an antibiotic cocktail developed a microbial biomass primarily composed of the pathogenic fungus that infiltrated the JC, resulting in severely reduced hatch rates. Experimental manipulation of the eggs demonstrated that the JC was protective against this fungal fouling. A large proportion of the bacterial strains isolated from the ANG or JC inhibited in culture (87.5%), while a similar proportion of extracts from these strains also exhibited antifungal activity against and/or the human-pathogenic yeast (72.7%). Mass spectral network analyses of active extracts from bacterial isolates and egg clutches revealed compounds that may be involved in preventing microbial overgrowth. Several secondary metabolites were identified from ANG/JC bacteria and egg clutches, including the known antimicrobial lincomycin as well as a suite of glycerophosphocholines and mycinamicin-like compounds. These results shed light on a widely distributed but poorly understood symbiosis in cephalopods and offer a new source for exploring bacterial secondary metabolites with antimicrobial activity. Organisms must have strategies to ensure successful reproduction. Some animals that deposit eggs protect their embryos from fouling/disease with the help of microorganisms. Although beneficial bacteria are hypothesized to contribute to egg defense in some organisms, the mechanisms of this protection remain largely unknown, with the exception of a few recently described systems. Using both experimental and analytical approaches, we demonstrate that symbiotic bacteria associated with a cephalopod reproductive gland and eggs inhibit fungi. Chemical analyses suggest that these bacteria produce antimicrobial compounds that may prevent overgrowth from fungi and other microorganisms. Given the distribution of these symbiotic glands among many cephalopods, similar defensive relationships may be more common in aquatic environments than previously realized. Such defensive symbioses may also be a rich source for the discovery of new antimicrobial compounds.
防御共生的重要性日益凸显，即在特定化合物的产生过程中，微生物通过保护宿主来发挥作用。尽管确定这些共生体中的伙伴变得更容易，但赋予这些关系功能通常是一个重大挑战。在这里，我们描述了夏威夷短尾乌贼生殖器官附属的细菌群落在保护生殖器官中的功能。细菌从附属的珠母腺（ANG）被分泌到卵果冻（JC）中，在那里它们被假设在胚胎发生过程中发挥防御作用。用抗生素鸡尾酒处理的卵孵化率严重降低，其卵果冻中主要由渗透到 JC 中的致病真菌组成的微生物生物量。实验性地处理这些卵表明，卵果冻可以防止这种真菌污染。从 ANG 或 JC 中分离出的大量细菌菌株在培养物中抑制了 （87.5%），而这些菌株的提取物也表现出对 和/或人类致病性酵母 的抗真菌活性（72.7%）。从细菌分离物和卵卵囊的活性提取物的质谱网络分析揭示了可能参与防止微生物过度生长的化合物。从 ANG/JC 细菌和卵卵囊中鉴定出几种次生代谢物，包括已知的抗菌药物林可霉素以及一系列甘油磷酸胆碱和 mycinamicin 样化合物。这些结果揭示了头足类动物中广泛存在但知之甚少的共生关系，并为探索具有抗菌活性的细菌次生代谢物提供了新的来源。生物必须有策略来确保成功繁殖。一些产卵动物在微生物的帮助下保护胚胎免受污染/疾病。虽然在一些生物中，有益细菌被假设为卵防御做出贡献，但这种保护的机制在很大程度上仍然未知，除了最近描述的几个系统。通过使用实验和分析方法，我们证明与头足类动物生殖腺和卵相关的共生细菌抑制真菌。化学分析表明，这些细菌产生的抗菌化合物可能防止真菌和其他微生物的过度生长。鉴于这些共生腺在许多头足类动物中的分布，类似的防御关系可能在水生环境中比以前认识到的更为普遍。这种防御共生关系也可能是发现新抗菌化合物的丰富来源。
