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. 2019 Oct 1;95(10):fiz146.
doi: 10.1093/femsec/fiz146.

Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico

Affiliations

Characterization of the microbiome and bioluminescent symbionts across life stages of Ceratioid Anglerfishes of the Gulf of Mexico

Lindsay L Freed et al. FEMS Microbiol Ecol. .

Abstract

The interdependence of diverse organisms through symbiosis reaches even the deepest parts of the oceans. As part of the DEEPEND project (deependconsortium.org) research on deep Gulf of Mexico biodiversity, we profiled the bacterial communities ('microbiomes') and luminous symbionts of 36 specimens of adult and larval deep-sea anglerfishes of the suborder Ceratioidei using 16S rDNA. Transmission electron microscopy was used to characterize the location of symbionts in adult light organs (esca). Whole larval microbiomes, and adult skin and gut microbiomes, were dominated by bacteria in the genera Moritella and Pseudoalteromonas. 16S rDNA sequencing results from adult fishes corroborate the previously published identity of ceratioid bioluminescent symbionts and support the findings that these symbionts do not consistently exhibit host specificity at the host family level. Bioluminescent symbiont amplicon sequence variants were absent from larval ceratioid samples, but were found at all depths in the seawater, with a highest abundance found at mesopelagic depths. As adults spend the majority of their lives in the meso- and bathypelagic zones, the trend in symbiont abundance is consistent with their life history. These findings support the hypothesis that bioluminescent symbionts are not present throughout host development, and that ceratioids acquire their bioluminescent symbionts from the environment.

Keywords: 16S rRNA; Ceratioidei; Gulf of Mexico; anglerfish microbiome; bioluminescence; symbiosis.

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Figures

Figure 1.
Figure 1.
(A) A M. johnsoni individual is shown on left, while a C. couesii sample is on the right. (B) Electron micrographs of layers within a C. couesii esca include an outer layer of epithelium tissue (ep), beneath this is a layer of densely packed cells containing bacteria (bc), and an inner layer of organic crystals (cry). (C) Epithelium tissue (ep) with individual bacteriocytes containing symbiont cells (bc). (D) The lower portion of the bacteriocytes (bc) showing contact with the layer of organic crystals (cry) in the center of the esca. (E) Random orientation of the presumably organic crystals (cry) in the center of the esca.
Figure 2.
Figure 2.
Boxplot of species richness and diversity comparing sample types based on observed richness (ANOVA, df = 7, F = 68.15, P = <0.001), Chao1 index (ANOVA, df = 7, F = 40.76, P = <0.001), Shannon index (ANOVA, df = 7, F = 89.5, P = <0.001) and Inverse Simpson index (ANOVA, df = 7, F = 20.51, P = <0.001).
Figure 3.
Figure 3.
NMDS of anglerfish and water samples. (R2 = 0.97, stress = 0.1699, solid ellipse = multivariate normal distribution with 95% CI).
Figure 4.
Figure 4.
(A) Bar plot of taxa present at >0.1% relative abundance within adult anglerfish specimens by Family. Anglerfish taxa are abbreviated as follows—Cryptopsaras couesii(CC), Melanocetus johnsonii(MJ), Melanocetus murrayi(MM), Centrophryne spinulosa (CSp), unknown Linophrynidae sp. (L), undefined Ceratias sp. (CU), unknown Oneirodes sp. (O), unknown Gigantactinidae sp (G). (B) Bar plot of taxa present at >0.1% relative abundance within larval anglerfish specimens by Family.
Figure 5.
Figure 5.
(A) Bar plot of Vibrionaceae ASVs within adult anglerfish specimens. Anglerfish taxa are abbreviated as in Fig. 4. (B) Bar plot of Vibrionaceae ASVs within juvenile anglerfish specimens.
Figure 6.
Figure 6.
Relative abundance of potential symbiont ASVs in seawater by Depth Zone. A total of 220 seawater samples (combining replicates) were analyzed. These samples were also described by Easson and Lopez (2018). Twenty-seven total samples were positive for E. luxaltus ASV and only one was positive for E. escacola.

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