1. Ecology
  2. Evolutionary Biology
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Diverse deep-sea anglerfishes share a genetically reduced luminous symbiont that is acquired from the environment

  1. Lydia J Baker  Is a corresponding author
  2. Lindsay L Freed
  3. Cole G Easson
  4. Jose V Lopez
  5. Danté Fenolio
  6. Tracey T Sutton
  7. Spencer V Nyholm
  8. Tory A Hendry  Is a corresponding author
  1. Cornell University, United States
  2. Nova Southeastern University, United States
  3. Middle Tennessee State University, United States
  4. Center for Conservation and Research, San Antonio Zoo, United States
  5. University of Connecticut, United States
Research Article
Cite this article as: eLife 2019;8:e47606 doi: 10.7554/eLife.47606
5 figures, 2 tables, 2 data sets and 7 additional files

Figures

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.

https://doi.org/10.7554/eLife.47606.003
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.

https://doi.org/10.7554/eLife.47606.005
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.

https://doi.org/10.7554/eLife.47606.006
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.

https://doi.org/10.7554/eLife.47606.007
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 ♦.

https://doi.org/10.7554/eLife.47606.008

Tables

Table 1
Statistics for symbiont genome sequences analyzed in this study.

Samples that are unique to this study are bolded. For binned genomes, the average nucleotide identity (ANI) of the genome compared to the reference sequence is shown. For E. luxaltus the reference was the CC26 symbiont and E. escacola was the MJ02 symbiont previously documented (Hendry et al., 2018). Results indicating similar species using ANI are bolded. Samples that could not be successfully binned and were not included in the ANI and completeness analysis are marked with a ‘--‘. Samples when compared to themselves are marked with ‘NA’. Statistics for total length and GC content were generated using OrthoANU, the percent completeness was generated using checkM, and the coverage was generated using BBmap. Sample location is denoted with a ♦ for those from the Northern Atlantic and without notation for those from the Gulf of Mexico.

https://doi.org/10.7554/eLife.47606.004
SampleFishIDLight
organ
Accession #E. escacola
ANI
E. luxaltus
ANI
Length
(Mb)
GC
content (%)
Complete (%)Ave coverage
CC26ECryptopsaras couesiiescaGCA002300443.173.7NA2.1437.791.325
CC32ECryptopsaras couesiiescaSRR8206628----------23
CC81CCryptopsaras couesiicaruncleSRR8206630----------19
CCS1ECryptopsaras couesiiescaRPOE0000000073.699.92.1437.790.8567
CCS2CCryptopsaras couesiicaruncleRPOF0000000073.799.92.2037.690.3313
CC62ECryptopsaras couesiiescaSRR8206629----------19
Csp75CCeratias uranoscopuscaruncleRPGC0000000099.973.82.7339.891.01600
CspS10CCeratias sp.caruncleRPGB0000000099.273.62.7239.891.199
CspS9CCeratias sp.caruncleRPGE0000000099.173.82.6939.889.326
CU44ECeratias uranoscopusescaRPGD0000000099.174.03.0439.888.315
CLS4EChaenophryne longcepsescaRPGF0000000099.973.72.7339.890.4330
CDS3EChaeonophryne sp.escaRPGG0000000099.973.62.7339.889.3291
LMS8ELinophryne maderensisescaRPGH0000000099.873.83.4040.088.81
MJ02EMelanocetus johnsoniescaGCA002381345.1NA73.72.6539.889.9766
MJS5xMelanocetus johnsoniescaRPGI0000000099.973.83.0939.891.1321
DP02EOneirodes sp.escaRPGJ00000000100.073.72.6839.889.3910
Table 2
A summary of modes of symbiont transmission, examples of some bacterial species and the functions they perform for animal hosts, and trends in the reduction of symbiont genomes.
https://doi.org/10.7554/eLife.47606.009
TransmissionDescriptionSymbiont and functionHostGenomeReferences
EnvironmentalAcquired from free-living bacteria
Luminescence
Aliivibrio fischeri
Photobacterium leiognathi
Photobacterium kishitanii
Nutrition
"Candidatus Endoriftia persephone"
Various Gammaproteobacteria
Burkholderia spp.

Fish and squid
Fish
Fish

Tubeworms
Mussels
Insects
Comprable to free-living relatives

Dunlap and Urbanczyk, 2013; Gyllborg et al., 2012
Urbanczyk et al., 2011; Ast et al., 2007
Li et al., 2018Kleiner et al., 2012
Ponnudurai et al., 2017
Kikuchi et al., 2005; Kikuchi et al., 2007
Proposed EnvironmentalEnvironmentally persistant cells


Luminescence
"Candidatus Enterovibrio escacola"
"Candidatus Enterovibrio luxaltus"

Anglerfish
Anglerfish
Ongoing reduction


Hendry et al., 2018
Hendry et al., 2018
MixedPseudovertical or surface transmission

Luminescence
"Candidatus Photodesmus blepharus"
"Candidatus Photodesmus katoptron"
Nutrition
Various Gammaproteobacteria
Candidatus Ishikawaella capsulata”

Flashlight fish
Flashlight fish

Clams
Stink bug
Moderate toextreme reduction

Hendry et al., 2014Hendry and Dunlap, 2014
Hendry et al., 2014Hendry and Dunlap, 2014

Kuwahara et al., 2007
InheritedDirect passage from parent to offspring on egg or sperm

Nutrition
Buchnera aphidicola
Carsonella ruddii
Portiera aleyrodidarum
Varied
"Candidatus Synechococcus spongiarum"

Aphids
Psyllids
Whiteflies

Sponges
Greatly reduced

Moran et al., 2008; Fisher et al., 2017
Moran et al., 2008Fisher et al., 2017
Moran et al., 2008Fisher et al., 2017

Gao et al., 2014; Burgsdorf et al., 2015

Data availability

The data used to generate figures can be found in the supplementary material, denoted by "S" in text. The symbiont genomes have been submitted to the SRA database and their accessions have been listed in Table 2 and Supplementary file 1. The fish mitochondrial sequences used in this study are listed in Supplementary file 2. Mitochondrial sequences generated in this study can be found in Genbank (MK118159-MK118174). The Vibrionaceae species used to generate Figure 1 are listed in Supplementary file 3. The Vibrionaceae species used to generate the conserved single-copy protein-coding genes is listed in Supplementary file 4. The bacterial species used to generate Figure 4 can be found in Supplementary file 6. The sequences produced as a result of this study are also listed and are in Genbank (MK457129-MK457136). All methods are outlined and all statistical analysis are described in detail in the manuscript such that they can be repeated.

The following data sets were generated
  1. 1
    NCBI BioProject
    1. A Hendry Tory
    2. J Baker Lydia
    (2018)
    ID PRJNA501852. Candidatus Enterovibrio luxaltus Genome sequencing and assembly.
  2. 2
    NCBI BioProject
    1. A Hendry Tory
    2. J Baker Lydia
    (2018)
    ID PRJNA501852. Diversity of anglerfish luminescent symbionts E. escacola.

Additional files

Supplementary file 1

Collection data for anglerfish samples used in this study.

Gulf of Mexico samples were collected by the DEEPEND consortium at the given locations. Samples collected by S. Nyholm were collected by RRS Discovery expedition D243 east of the Cape Verde Islands at the given locations. A single sample (DP02E) was given a new taxonomic identification as a result of mitochondrial gene analysis.

https://doi.org/10.7554/eLife.47606.010
Supplementary file 2

Lophiiform mitochondrial sequences used in this study.

Genbank accession numbers and total sequence length are shown. Samples listed in bold were generated by this study or by Hendry et al. (2018).

https://doi.org/10.7554/eLife.47606.011
Supplementary file 3

Sequences from free-living Vibrionaceae species used to generate the housekeeping gene tree.

Genbank accession numbers of each gene are given.

https://doi.org/10.7554/eLife.47606.012
Supplementary file 4

Genomes from free-living Vibrionaceae species used for PhyloPhlan analysis.

Genbank accession numbers of each genome assembly are given.

https://doi.org/10.7554/eLife.47606.013
Supplementary file 5

The species-specific primers designed to amplify the chemotaxis protein cheA.

https://doi.org/10.7554/eLife.47606.014
Supplementary file 6

Species-specific primers designed to amplify the chemotaxis protein cheA.

https://doi.org/10.7554/eLife.47606.015
Transparent reporting form
https://doi.org/10.7554/eLife.47606.016

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