Genome erosion and evidence for an intracellular niche – exploring the biology of mycoplasmas in Atlantic salmon
Mycoplasmas are the smallest autonomously self-replicating life form on the planet. Members of this bacterial genus are known to parasitise a wide array of metazoans including vertebrates. Whilst much research has been significant targeted at parasitic mammalian mycoplasmas, very little is known abo...
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creator | Cheaib, B. Yang, P. Kazlauskaite, R. Lindsay, E. Heys, C. Dwyer, T. De Noia, M. Schaal, Patrick Sloan, W. Ijaz, U.Z. Llewellyn, M.S. |
description | Mycoplasmas are the smallest autonomously self-replicating life form on the planet. Members of this bacterial genus are known to parasitise a wide array of metazoans including vertebrates. Whilst much research has been significant targeted at parasitic mammalian mycoplasmas, very little is known about their role in other vertebrates. In the current study, we aim to explore the biology of mycoplasmas in Atlantic Salmon, a species of major significance for aquaculture, including cellular niche, genome size structure and gene content. Using fluorescent in-situ hybridisation (FISH), mycoplasmas were targeted in epithelial tissues across the digestive tract (stomach, pyloric caecum and midgut) from different development stages (eggs, parr, subadult) of farmed Atlantic salmon (Salmo salar), and we present evidence for an intracellular niche for some of the microbes visualised. Via shotgun metagenomic sequencing, a nearly complete, albeit small, genome (~0.57 MB) as assembled from a farmed Atlantic salmon subadult. Phylogenetic analysis of the recovered genome revealed taxonomic proximity to other salmon derived mycoplasmas, as well as to the human pathogen Mycoplasma penetrans (~1.36 Mb). We annotated coding sequences and identified riboflavin pathway encoding genes and sugar transporters, the former potentially consistent with micronutrient provisioning in salmonid development. Our study provides insights into mucosal adherence, the cellular niche and gene catalog of Mycoplasma in the gut ecosystem of the Atlantic salmon, suggesting a high dependency of this minimalist bacterium on its host. Further study is required to explore and functional role of Mycoplasma in the nutrition and development of its salmonid host.
•Mycoplasmas colonize the epithelial niche of the Atlantic salmon GI tract through its different development stages.•A nearly complete, albeit small, genome (~0.57 MB) assembled from Atlantic salmon subadult suggests genome reduction.•The lack of mobile genes and virulence factors in the mycoplasma genome could support a non-pathogenic lifestyle.•Mycoplasma’s genome content suggests role for host nutrient provisioning relevance to aquaculture.•Shotgun metagenomics, phylogenetics, and fluorescence in situ hybridization are relevant methods in aquaculture research. |
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•Mycoplasmas colonize the epithelial niche of the Atlantic salmon GI tract through its different development stages.•A nearly complete, albeit small, genome (~0.57 MB) assembled from Atlantic salmon subadult suggests genome reduction.•The lack of mobile genes and virulence factors in the mycoplasma genome could support a non-pathogenic lifestyle.•Mycoplasma’s genome content suggests role for host nutrient provisioning relevance to aquaculture.•Shotgun metagenomics, phylogenetics, and fluorescence in situ hybridization are relevant methods in aquaculture research.</description><identifier>ISSN: 0044-8486</identifier><identifier>EISSN: 1873-5622</identifier><identifier>EISSN: 0044-8486</identifier><identifier>DOI: 10.1016/j.aquaculture.2021.736772</identifier><identifier>PMID: 34471330</identifier><language>eng</language><publisher>Elsevier B.V</publisher><ispartof>Aquaculture, 2021-08, Vol.541, p.736772-736772, Article 736772</ispartof><rights>2021 The Author(s)</rights><rights>2021 The Author(s) 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c460t-fe10b1083134ad068d182bee8229af147a744852345c4a177930d4d35cdd70b03</citedby><cites>FETCH-LOGICAL-c460t-fe10b1083134ad068d182bee8229af147a744852345c4a177930d4d35cdd70b03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.aquaculture.2021.736772$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids></links><search><creatorcontrib>Cheaib, B.</creatorcontrib><creatorcontrib>Yang, P.</creatorcontrib><creatorcontrib>Kazlauskaite, R.</creatorcontrib><creatorcontrib>Lindsay, E.</creatorcontrib><creatorcontrib>Heys, C.</creatorcontrib><creatorcontrib>Dwyer, T.</creatorcontrib><creatorcontrib>De Noia, M.</creatorcontrib><creatorcontrib>Schaal, Patrick</creatorcontrib><creatorcontrib>Sloan, W.</creatorcontrib><creatorcontrib>Ijaz, U.Z.</creatorcontrib><creatorcontrib>Llewellyn, M.S.</creatorcontrib><title>Genome erosion and evidence for an intracellular niche – exploring the biology of mycoplasmas in Atlantic salmon</title><title>Aquaculture</title><description>Mycoplasmas are the smallest autonomously self-replicating life form on the planet. Members of this bacterial genus are known to parasitise a wide array of metazoans including vertebrates. Whilst much research has been significant targeted at parasitic mammalian mycoplasmas, very little is known about their role in other vertebrates. In the current study, we aim to explore the biology of mycoplasmas in Atlantic Salmon, a species of major significance for aquaculture, including cellular niche, genome size structure and gene content. Using fluorescent in-situ hybridisation (FISH), mycoplasmas were targeted in epithelial tissues across the digestive tract (stomach, pyloric caecum and midgut) from different development stages (eggs, parr, subadult) of farmed Atlantic salmon (Salmo salar), and we present evidence for an intracellular niche for some of the microbes visualised. Via shotgun metagenomic sequencing, a nearly complete, albeit small, genome (~0.57 MB) as assembled from a farmed Atlantic salmon subadult. Phylogenetic analysis of the recovered genome revealed taxonomic proximity to other salmon derived mycoplasmas, as well as to the human pathogen Mycoplasma penetrans (~1.36 Mb). We annotated coding sequences and identified riboflavin pathway encoding genes and sugar transporters, the former potentially consistent with micronutrient provisioning in salmonid development. Our study provides insights into mucosal adherence, the cellular niche and gene catalog of Mycoplasma in the gut ecosystem of the Atlantic salmon, suggesting a high dependency of this minimalist bacterium on its host. Further study is required to explore and functional role of Mycoplasma in the nutrition and development of its salmonid host.
•Mycoplasmas colonize the epithelial niche of the Atlantic salmon GI tract through its different development stages.•A nearly complete, albeit small, genome (~0.57 MB) assembled from Atlantic salmon subadult suggests genome reduction.•The lack of mobile genes and virulence factors in the mycoplasma genome could support a non-pathogenic lifestyle.•Mycoplasma’s genome content suggests role for host nutrient provisioning relevance to aquaculture.•Shotgun metagenomics, phylogenetics, and fluorescence in situ hybridization are relevant methods in aquaculture research.</description><issn>0044-8486</issn><issn>1873-5622</issn><issn>0044-8486</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><recordid>eNqNkc9uEzEQxi0EoiHwDubGJcH_1vZekKoI2kqVuMDZ8tqzqSOvndq7Ebn1HXhDnoRdpUJw4zTSzHzfaH4fQu8p2VJC5cfD1j5O1k1xnApsGWF0q7hUir1AK6oV3zSSsZdoRYgQGy20vEJvaj0QQqRs6Gt0xYVQlHOyQuUGUh4AQ8k15IRt8hhOwUNygPtc5gYOaSzWQYxTtAWn4B4A_3r6ieHHMeYS0h6Pc6cLOeb9GeceD2eXj9HWwdZZjK_HaNMYHK42Djm9Ra96Gyu8e65r9P3L52-7283915u73fX9xglJxk0PlHSUaE65sJ5I7almHYBmrLU9FcoqIXTDuGicsFSplhMvPG-c94p0hK_Rp4vvceoG8A6WN6I5ljDYcjbZBvPvJIUHs88no2nLxIxnjT48G5T8OEEdzRDqwsEmyFM1rJG6aZUUYl5tL6tu5lgL9H_OUGKWzMzB_JWZWTIzl8xm7e6ihRnGKUAx1YWFvw8F3Gh8Dv_h8htHn6fj</recordid><startdate>20210830</startdate><enddate>20210830</enddate><creator>Cheaib, B.</creator><creator>Yang, P.</creator><creator>Kazlauskaite, R.</creator><creator>Lindsay, E.</creator><creator>Heys, C.</creator><creator>Dwyer, T.</creator><creator>De Noia, M.</creator><creator>Schaal, Patrick</creator><creator>Sloan, W.</creator><creator>Ijaz, U.Z.</creator><creator>Llewellyn, M.S.</creator><general>Elsevier B.V</general><general>Elsevier Pub. Co</general><scope>6I.</scope><scope>AAFTH</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20210830</creationdate><title>Genome erosion and evidence for an intracellular niche – exploring the biology of mycoplasmas in Atlantic salmon</title><author>Cheaib, B. ; Yang, P. ; Kazlauskaite, R. ; Lindsay, E. ; Heys, C. ; Dwyer, T. ; De Noia, M. ; Schaal, Patrick ; Sloan, W. ; Ijaz, U.Z. ; Llewellyn, M.S.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c460t-fe10b1083134ad068d182bee8229af147a744852345c4a177930d4d35cdd70b03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cheaib, B.</creatorcontrib><creatorcontrib>Yang, P.</creatorcontrib><creatorcontrib>Kazlauskaite, R.</creatorcontrib><creatorcontrib>Lindsay, E.</creatorcontrib><creatorcontrib>Heys, C.</creatorcontrib><creatorcontrib>Dwyer, T.</creatorcontrib><creatorcontrib>De Noia, M.</creatorcontrib><creatorcontrib>Schaal, Patrick</creatorcontrib><creatorcontrib>Sloan, W.</creatorcontrib><creatorcontrib>Ijaz, U.Z.</creatorcontrib><creatorcontrib>Llewellyn, M.S.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Aquaculture</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cheaib, B.</au><au>Yang, P.</au><au>Kazlauskaite, R.</au><au>Lindsay, E.</au><au>Heys, C.</au><au>Dwyer, T.</au><au>De Noia, M.</au><au>Schaal, Patrick</au><au>Sloan, W.</au><au>Ijaz, U.Z.</au><au>Llewellyn, M.S.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Genome erosion and evidence for an intracellular niche – exploring the biology of mycoplasmas in Atlantic salmon</atitle><jtitle>Aquaculture</jtitle><date>2021-08-30</date><risdate>2021</risdate><volume>541</volume><spage>736772</spage><epage>736772</epage><pages>736772-736772</pages><artnum>736772</artnum><issn>0044-8486</issn><eissn>1873-5622</eissn><eissn>0044-8486</eissn><abstract>Mycoplasmas are the smallest autonomously self-replicating life form on the planet. Members of this bacterial genus are known to parasitise a wide array of metazoans including vertebrates. Whilst much research has been significant targeted at parasitic mammalian mycoplasmas, very little is known about their role in other vertebrates. In the current study, we aim to explore the biology of mycoplasmas in Atlantic Salmon, a species of major significance for aquaculture, including cellular niche, genome size structure and gene content. Using fluorescent in-situ hybridisation (FISH), mycoplasmas were targeted in epithelial tissues across the digestive tract (stomach, pyloric caecum and midgut) from different development stages (eggs, parr, subadult) of farmed Atlantic salmon (Salmo salar), and we present evidence for an intracellular niche for some of the microbes visualised. Via shotgun metagenomic sequencing, a nearly complete, albeit small, genome (~0.57 MB) as assembled from a farmed Atlantic salmon subadult. Phylogenetic analysis of the recovered genome revealed taxonomic proximity to other salmon derived mycoplasmas, as well as to the human pathogen Mycoplasma penetrans (~1.36 Mb). We annotated coding sequences and identified riboflavin pathway encoding genes and sugar transporters, the former potentially consistent with micronutrient provisioning in salmonid development. Our study provides insights into mucosal adherence, the cellular niche and gene catalog of Mycoplasma in the gut ecosystem of the Atlantic salmon, suggesting a high dependency of this minimalist bacterium on its host. Further study is required to explore and functional role of Mycoplasma in the nutrition and development of its salmonid host.
•Mycoplasmas colonize the epithelial niche of the Atlantic salmon GI tract through its different development stages.•A nearly complete, albeit small, genome (~0.57 MB) assembled from Atlantic salmon subadult suggests genome reduction.•The lack of mobile genes and virulence factors in the mycoplasma genome could support a non-pathogenic lifestyle.•Mycoplasma’s genome content suggests role for host nutrient provisioning relevance to aquaculture.•Shotgun metagenomics, phylogenetics, and fluorescence in situ hybridization are relevant methods in aquaculture research.</abstract><pub>Elsevier B.V</pub><pmid>34471330</pmid><doi>10.1016/j.aquaculture.2021.736772</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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title | Genome erosion and evidence for an intracellular niche – exploring the biology of mycoplasmas in Atlantic salmon |
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