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

Baker, L.; Freed, Lindsay L; Easson, Cole G.; Lopez, Jose V.; Fenolio, Danté B.; Sutton, Tracey; Nyholm, Spencer V.; Hendry, Tory A.

doi:10.7554/elife.47606

Cited by 34 publications

(30 citation statements)

References 100 publications

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“…It is perhaps surprising that the most dominant members of C. delitrix microbiomes are potentially acquired from the environment, rather than vertically transmitted. If these taxa are horizontally transmitted, C. delitrix juveniles must have a mechanism for selecting these specific taxa out of the vast number that exist in the environment similar to those mechanisms in other symbiotic systems (Baker et al, ; Mcfall‐Ngai, ; Nyholm & McFall‐Ngai, ).…”

Section: Discussionmentioning

confidence: 99%

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Easson

Chaves‐Fonnegra

Thacker

et al. 2020

Ecology and Evolution

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Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (<300 km) was observed. Host population structure had a moderate effect on the structure of these microbial communities, regardless of geographic distance. These results support the interplay between geographic, environmental, and host factors as forces determining the community structure of microbiomes associated with C. delitrix. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.

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Section: Discussionmentioning

confidence: 99%

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Easson

Chaves‐Fonnegra

Thacker

et al. 2020

Ecology and Evolution

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“…It is remarkable that strain MT41 and MTCD1, two piezophiles isolated from amphipod material in the Mariana Trench 34 years apart, share over 99% ANI. Perhaps this reflects strong selection for a particular Colwellia strain within the microbiome of Mariana Trench Hirondellea gigas amphipods, such as that seen within symbionts of deep-sea anglerfishes [ 9 ]. Their consistent isolation from amphipods (e.g.…”

Section: Discussionmentioning

confidence: 99%

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

et al. 2020

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Background The deep ocean is characterized by low temperatures, high hydrostatic pressures, and low concentrations of organic matter. While these conditions likely select for distinct genomic characteristics within prokaryotes, the attributes facilitating adaptation to the deep ocean are relatively unexplored. In this study, we compared the genomes of seven strains within the genus Colwellia, including some of the most piezophilic microbes known, to identify genomic features that enable life in the deep sea. Results Significant differences were found to exist between piezophilic and non-piezophilic strains of Colwellia. Piezophilic Colwellia have a more basic and hydrophobic proteome. The piezophilic abyssal and hadal isolates have more genes involved in replication/recombination/repair, cell wall/membrane biogenesis, and cell motility. The characteristics of respiration, pilus generation, and membrane fluidity adjustment vary between the strains, with operons for a nuo dehydrogenase and a tad pilus only present in the piezophiles. In contrast, the piezosensitive members are unique in having the capacity for dissimilatory nitrite and TMAO reduction. A number of genes exist only within deep-sea adapted species, such as those encoding d-alanine-d-alanine ligase for peptidoglycan formation, alanine dehydrogenase for NADH/NAD+ homeostasis, and a SAM methyltransferase for tRNA modification. Many of these piezophile-specific genes are in variable regions of the genome near genomic islands, transposases, and toxin-antitoxin systems. Conclusions We identified a number of adaptations that may facilitate deep-sea radiation in members of the genus Colwellia, as well as in other piezophilic bacteria. An enrichment in more basic and hydrophobic amino acids could help piezophiles stabilize and limit water intrusion into proteins as a result of high pressure. Variations in genes associated with the membrane, including those involved in unsaturated fatty acid production and respiration, indicate that membrane-based adaptations are critical for coping with high pressure. The presence of many piezophile-specific genes near genomic islands highlights that adaptation to the deep ocean may be facilitated by horizontal gene transfer through transposases or other mobile elements. Some of these genes are amenable to further study in genetically tractable piezophilic and piezotolerant deep-sea microorganisms.

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“…Histological study and genome sequence analyses of Cryptopsaras couesii caruncle symbionts, like the esca, contain dense populations of luminous bacteria that can be expelled through a distal pore (Herring and Morin 1978; Hansen and Herring 2009; Baker et al. in press).…”

Section: Introductionmentioning

confidence: 99%

“…Although these patterns are common to vertically transmitted symbionts (Bright and Bulgheresi 2010; McCutcheon and Moran 2012), recent work found support for the hypothesis that anglerfish acquire their symbionts from environmental populations (Freed 2018; Baker et al . in press). This style of environmental transmission is also found in most other symbiotically luminous fishes (Dunlap et al .…”

Section: Introductionmentioning

confidence: 99%

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

Freed

Easson

Baker

et al. 2019

FEMS Microbiology Ecology

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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.

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

Cited by 34 publications

References 100 publications

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Distinctive gene and protein characteristics of extremely piezophilic Colwellia

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

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