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

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          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.

          Abstract

          Molecular characterization of bioluminescent bacterial symbionts and comparison with bacteria at other body parts in six families of anglerfish of the Gulf of Mexico.

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          Most cited references36

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          Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample.

          The ongoing revolution in high-throughput sequencing continues to democratize the ability of small groups of investigators to map the microbial component of the biosphere. In particular, the coevolution of new sequencing platforms and new software tools allows data acquisition and analysis on an unprecedented scale. Here we report the next stage in this coevolutionary arms race, using the Illumina GAIIx platform to sequence a diverse array of 25 environmental samples and three known "mock communities" at a depth averaging 3.1 million reads per sample. We demonstrate excellent consistency in taxonomic recovery and recapture diversity patterns that were previously reported on the basis of metaanalysis of many studies from the literature (notably, the saline/nonsaline split in environmental samples and the split between host-associated and free-living communities). We also demonstrate that 2,000 Illumina single-end reads are sufficient to recapture the same relationships among samples that we observe with the full dataset. The results thus open up the possibility of conducting large-scale studies analyzing thousands of samples simultaneously to survey microbial communities at an unprecedented spatial and temporal resolution.
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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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              Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents.

              The newly established genus Pseudoalteromonas contains numerous marine species which synthesize biologically active molecules. The production of a range of compounds which are active against a variety of target organisms appears to be a unique characteristic for this genus and may greatly benefit Pseudoalteromonas cells in their competition for nutrients and colonization of surfaces. Species of Pseudoalteromonas are generally found in association with marine eukaryotes and display anti-bacterial, bacteriolytic, agarolytic and algicidal activities. Moreover, several Pseudoalteromonas isolates specifically prevent the settlement of common fouling organisms. While a wide range of inhibitory extracellular agents are produced, compounds promoting the survival of other marine organisms living in the vicinity of Pseudoalteromonas species have also been found.
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                Author and article information

                Journal
                FEMS Microbiol Ecol
                FEMS Microbiol. Ecol
                femsec
                FEMS Microbiology Ecology
                Oxford University Press
                0168-6496
                1574-6941
                10 September 2019
                October 2019
                10 September 2019
                : 95
                : 10
                : fiz146
                Affiliations
                [1 ] Halmos College of Natural Sciences and Oceanography, Nova Southeastern University , Dania Beach, FL, 33004 USA
                [2 ] Department of Microbiology, Cornell University , Ithaca, NY, 14850 USA
                [3 ] Center for Conservation and Research, San Antonio Zoo , San Antonio, TX, 78212 USA
                [4 ] University of Miami Center for Advanced Microscopy, Department of Chemistry, University of Miami , Coral Gables, FL, 33146 USA
                Author notes
                Corresponding author: Department of Biological Sciences, Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, 8000 N. Ocean Dr. Dania Beach FL 33004. E-mail: joslo@ 123456nova.edu
                Author information
                http://orcid.org/0000-0002-8001-1783
                http://orcid.org/0000-0002-1637-4125
                Article
                fiz146
                10.1093/femsec/fiz146
                6778416
                31504465
                a748be3b-07f5-4d00-b74d-cf41fe001d3a
                © FEMS 2019.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                : 11 June 2019
                : 09 September 2019
                Page count
                Pages: 11
                Funding
                Funded by: Gulf of Mexico Research Initiative 10.13039/100007240
                Categories
                Research Article

                Microbiology & Virology
                gulf of mexico,ceratioidei,16s rrna,bioluminescence,symbiosis,anglerfish microbiome

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