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. 2019 Oct 1:8:e47606.
doi: 10.7554/eLife.47606.

Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment

Lydia J Baker  1 , Lindsay L Freed  2 , Cole G Easson  2   3 , Jose V Lopez  2 , Danté Fenolio  4 , Tracey T Sutton  2 , Spencer V Nyholm  5 , Tory A Hendry  1
Affiliations

Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment

Lydia J Baker et al. Elife. .

Abstract

Deep-sea anglerfishes are relatively abundant and diverse, but their luminescent bacterial symbionts remain enigmatic. The genomes of two symbiont species have qualities common to vertically transmitted, host-dependent bacteria. However, a number of traits suggest that these symbionts may be environmentally acquired. To determine how anglerfish symbionts are transmitted, we analyzed bacteria-host codivergence across six diverse anglerfish genera. Most of the anglerfish species surveyed shared a common species of symbiont. Only one other symbiont species was found, which had a specific relationship with one anglerfish species, Cryptopsaras couesii. Host and symbiont phylogenies lacked congruence, and there was no statistical support for codivergence broadly. We also recovered symbiont-specific gene sequences from water collected near hosts, suggesting environmental persistence of symbionts. Based on these results we conclude that diverse anglerfishes share symbionts that are acquired from the environment, and that these bacteria have undergone extreme genome reduction although they are not vertically transmitted.

Keywords: bioluminescent symbiosis; deep-sea anglerfishes; ecology; evolutionary biology; host-symbiont codivergence; none; symbiont transmission.

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Conflict of interest statement

LB, LF, CE, JL, DF, TS, SN, TH No competing interests declared

Figures

Figure 1.
Figure 1.. Maximum likelihood phylogenetic tree of bacterial symbionts from conserved housekeeping genes: 16S rDNA, atpA, gapA, gyrB, rpoA, and topA.
General time reversible was selected by modelfinder and a tree was constructed using IQ-TREE with 1000 bootstrap replicates. Those samples unique to this study are bolded, with samples from the Northern Atlantic denoted with ♦, and the bootstrap values over 60 are listed at tree nodes.
Figure 2.
Figure 2.. Symbiont phylogeny (left) constructed using single-copy protein-coding genes compared to the host phylogeny constructed using mitochondrial genes (right).
Bolded samples are unique to this study. Samples from the Northern Atlantic denoted with ♦, and the bootstrap values over 60 are listed at tree nodes. Linkages between symbionts and their hosts are shown with dotted lines that differentiate between symbiont species.
Figure 3.
Figure 3.. Procrustean Approach to Cophylogeny using a host matrix constructed using mitochondrial gene phylogeny compared to symbiont matrices constructed using the single-copy protein-coding gene phylogeny (p=2e-05) and housekeeping genes phylogeny (p=2e-05).
SNPs phylogenies were analyzed for each species, and the scale for E. luxaltus was dissimilar to the E. ecacola; neither were statistically significant (p>0.5 for analysis of both species). The squared residuals below the median squared residual value (dotted line) are significantly codiverging with the host phylogenies (marked with an asterisk). Sample IDs from the Northern Atlantic are marked with a ♦ and those from the Gulf of Mexico are unmarked.
Figure 4.
Figure 4.. Maximum likelihood phylogenetic tree of cheAfrom environmental samples (bolded) compared to sequences from symbiont genomes isolated from fish and sequences from related species.
Modelfinder selected the general time reversible model and a tree was constructed using IQ-TREE with 1000 bootstrap replicates. Those samples from the Northern Atlantic denoted with ♦, and the bootstrap values over 60 are given at tree nodes.
Figure 5.
Figure 5.. Phylogenies constructed using single nucleotide polymorphisms for (A) E. luxaltus (2252 SNPs) and (B) E. escacola (15272 SNPs).
Host identifications for each sample are listed in the right-hand column. Samples unique to this study are bolded and those from the Northern Atlantic are marked with a ♦.
See this image and copyright information in PMC

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