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

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          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.

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          The deep sea is home to many different species of anglerfish, a group of animals in which females often display a dangling lure on the top of their heads. This organ shelters bacteria that make light, a partnership (known as symbiosis) that benefits both parties. The bacteria get a safe environment in which to grow, while the animal may use the light to confuse predators as well as attract prey and mates.

          The genetic information of these bacteria has changed since they became associated with their host. Their genomes have become smaller and more specialized, limiting their ability to survive outside of the fish. This phenomenon is also observed in other symbiotic bacteria, but mostly in microorganisms that are directly transmitted from parent to offspring, never having to live on their own. Yet, some evidence suggests that the bacteria in the lure of anglerfish may be spending time in the water until they find a new host, crossing thousands of meters of ocean in the process.

          To explore this paradox, Baker et al. looked into the type of bacteria carried by different groups of anglerfish. If each type of fish has its own kind of bacteria, this would suggest that the microorganisms are passed from one generation to the next, and are evolving with their hosts. On the other hand, if the same sort of bacteria can be found in different anglerfish species, this would imply that the bacteria pass from host to host and evolve independently from the fish.

          Genetic data analysis showed that amongst six groups of anglerfishes, one species of bacteria is shared across five groups while another is specific to one type of fish. The analyses also revealed that anglerfish and their bacteria are most likely not evolving together. This means that the bacteria must make the difficult journey from host to host by persisting in the deep sea, which was confirmed by finding the genetic information of these bacteria in the water near the fish.

          Anglerfish and the bacteria that light up their lure are hard to study, as they live so deep in the ocean. In fact, many symbiotic relationships are equally difficult to investigate. Examining genetic information can help to give an insight into how hosts and bacteria interact across the tree of life.

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          Most cited references73

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          Extreme genome reduction in symbiotic bacteria.

          Since 2006, numerous cases of bacterial symbionts with extraordinarily small genomes have been reported. These organisms represent independent lineages from diverse bacterial groups. They have diminutive gene sets that rival some mitochondria and chloroplasts in terms of gene numbers and lack genes that are considered to be essential in other bacteria. These symbionts have numerous features in common, such as extraordinarily fast protein evolution and a high abundance of chaperones. Together, these features point to highly degenerate genomes that retain only the most essential functions, often including a considerable fraction of genes that serve the hosts. These discoveries have implications for the concept of minimal genomes, the origins of cellular organelles, and studies of symbiosis and host-associated microbiota.
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            Learning how to live together: genomic insights into prokaryote-animal symbioses.

            Our understanding of prokaryote-eukaryote symbioses as a source of evolutionary innovation has been rapidly increased by the advent of genomics, which has made possible the biological study of uncultivable endosymbionts. Genomics is allowing the dissection of the evolutionary process that starts with host invasion then progresses from facultative to obligate symbiosis and ends with replacement by, or coexistence with, new symbionts. Moreover, genomics has provided important clues on the mechanisms driving the genome-reduction process, the functions that are retained by the endosymbionts, the role of the host, and the factors that might determine whether the association will become parasitic or mutualistic.
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              Aligning Sequence Reads, Clone Sequences and Assembly Contigs with BWA-MEM

              H. Li, Li, H Li (2013)
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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                01 October 2019
                2019
                : 8
                : e47606
                Affiliations
                [1 ]deptDepartment of Microbiology Cornell University New YorkUnited States
                [2 ]deptHalmos College of Natural Sciences and Oceanography Nova Southeastern University Fort LauderdaleUnited States
                [3 ]deptDepartment of Biology Middle Tennessee State University MurfreesboroUnited States
                [4 ]Center for Conservation and Research, San Antonio Zoo San AntonioUnited States
                [5 ]deptDepartment of Molecular and Cell Biology University of Connecticut StorrsUnited States
                University of Michigan United States
                University of Michigan United States
                University of Michigan United States
                Author information
                https://orcid.org/0000-0002-1453-421X
                https://orcid.org/0000-0002-1637-4125
                https://orcid.org/0000-0002-8001-1783
                Article
                47606
                10.7554/eLife.47606
                6773444
                31571583
                262b8acf-07bb-473c-9c2d-c8c45652fccb
                © 2019, Baker et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 11 April 2019
                : 21 August 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100007240, Gulf of Mexico Research Initiative;
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Ecology
                Evolutionary Biology
                Custom metadata
                Environmental transmission is atypical of symbionts that have undergone genome degradation, yet genetically reduced deep-sea anglerfish symbionts likely persist in the deep sea biome in search of a new host.

                Life sciences
                symbiont transmission,host-symbiont codivergence,bioluminescent symbiosis,deep-sea anglerfishes,none

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