Microbiomes and Dynamic Genomes of Anglerfish Bacterial Symbionts in the Gulf of Mexico

Guy Harvey Oceanographic Center Facility

As part of the Gulf of Mexico Research Initiative (GOMRI)-funded DEEPEND project (Deependconsortium.org), our laboratory has focused on the intersection of microbiology and deep-sea anglerfish. Many female deep-sea anglerfishes possess a “lure” (esca) containing extracellular luminous bacterial symbionts. We first intended to determine whether symbiotic microbes were specific to anglerfish hosts in the GOM, to the esca itself and distinct from surrounding seawater. Anglerfish specimens were collected and identified on DEEPEND cruises DP01 through DP04. These specimens consisted of adult and larval individuals belonging to six of the families of suborder Ceratioidei: Ceratiidae, Centrophrynidae, Melanocetidae, Oneirodidae, Gigantactinidae, Linophrynidae. Genomic DNA was extracted from esca, skin, fin, gill, gut, larval (caruncle) samples as well as seawater for comparison. High-throughput sequencing of the hypervariable V4 region of the 16S rRNA gene was carried out using the Illumina MiSeq. The lures of each anglerfish species were primarily dominated by a few OTUs. By contrast, non-escal organs did not reveal dominant microbes or any strong specific patterns similar to esca. However, preliminary results hint at possible horizontal connections between anglerfish and their surrounding environment. Secondly, the unique symbiont taxa identified from DP01 and DP02 samples led to whole symbiont genome characterizations by our Cornell University collaborators. We show that unlike most luminous symbionts, which are facultatively host-associated, these bacteria are undergoing genome reduction. Deep-sea anglerfish symbiont genomes appear reduced in size by about 50% compared to free-living relatives and possess limited metabolic capabilities. However, gene composition and retention allowed inferences of possible ecological lifestyles of symbionts. Categories ofsome retained genes are predicted to be adaptive outside of the host, such as those involved in chemotaxis and motility, others are suggestive of dependence on the host fish. The symbiont genomes contain unexpectedly high numbers of pseudogenes and show massive expansions of transposable elements, with transposases accounting for up to 31% of coding sequences in the symbiont genomes. Transposon expansions appear to have occurred at different times in each symbiont, indicating independent evolutions of reduction or symbiont replacement. These results suggest dynamic and ongoing genomic reduction in these extracellular symbionts.