Abstract
Female members of many cephalopod species house a bacterial consortium in the accessory nidamental gland (ANG), part of the reproductive system. These bacteria are deposited into eggs that are then laid in the environment where they must develop unprotected from predation, pathogens, and fouling. In this study, we characterized the genome and secondary metabolite production of Leisingera sp. JC1, a member of the roseobacter clade (Rhodobacteraceae) of Alphaproteobacteria isolated from the jelly coat of eggs from the Hawaiian bobtail squid, Euprymna scolopes. Whole genome sequencing and MLSA analysis revealed that Leisingera sp. JC1 falls within a group of roseobacters associated with squid ANGs. Genome and biochemical analyses revealed the potential for and production of a number of secondary metabolites, including siderophores and acyl-homoserine lactones involved with quorum sensing. The complete biosynthetic gene cluster for the pigment indigoidine was detected in the genome and mass spectrometry confirmed the production of this compound. Furthermore, we investigated the production of indigoidine under co-culture conditions with Vibrio fischeri, the light organ symbiont of E. scolopes, and with other vibrios. Finally, both Leisingera sp. JC1 and secondary metabolite extracts of this strain had differential antimicrobial activity against a number of marine vibrios, suggesting that Leisingera sp. JC1 may play a role in host defense against other marine bacteria either in the eggs and/or ANG. These data also suggest that indigoidine may be partially, but not wholly, responsible for the antimicrobial activity of this squid-associated bacterium.
Highlights
It is becoming increasingly evident that many animals and plants use compounds produced by symbiotic bacteria for protection against pathogens and other fouling organisms
One common yet poorly understood animal–bacterial association occurs between members of squid and cuttlefish species and bacterial consortia that reside within a reproductive gland of female hosts called the accessory nidamental gland (ANG; Kaufman et al, 1998; Grigioni et al, 2000; Barbieri et al, 2001; Pichon et al, 2005; Collins et al, 2012)
JC1 has a draft genome size of 5.19 Mb and GC content of 62.3% (Table 1), which is average for members of the roseobacter clade and similar to other squid-associated isolates (Collins et al, 2015)
Summary
It is becoming increasingly evident that many animals and plants use compounds produced by symbiotic bacteria for protection against pathogens and other fouling organisms (reviewed in Flórez et al, 2015). One common yet poorly understood animal–bacterial association occurs between members of squid and cuttlefish species and bacterial consortia that reside within a reproductive gland of female hosts called the accessory nidamental gland (ANG; Kaufman et al, 1998; Grigioni et al, 2000; Barbieri et al, 2001; Pichon et al, 2005; Collins et al, 2012) This organ harbors a dense consortium of bacteria housed in epithelium-lined tubules that are attached to the nidamental gland, the organ that secretes the jelly coat (JC) surrounding fertilized eggs. Bacteria from the ANG are deposited into the JC where they have been hypothesized to help protect developing eggs from fouling microorganisms, pathogens, and/or predation (Barbieri et al, 1997, 2001; Collins et al, 2012, 2015)
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