Inducing novel endosymbioses by implanting bacteria in fungi
Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification 1 , 2 . Despite the many examples of known endosymbioses across the tr...
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creator | Giger, Gabriel H. Ernst, Chantal Richter, Ingrid Gassler, Thomas Field, Christopher M. Sintsova, Anna Kiefer, Patrick Gäbelein, Christoph G. Guillaume–Gentil, Orane Scherlach, Kirstin Bortfeld-Miller, Miriam Zambelli, Tomaso Sunagawa, Shinichi Künzler, Markus Hertweck, Christian Vorholt, Julia A. |
description | Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification
1
,
2
. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect
3
–
5
. Here we implant bacteria into the filamentous fungus
Rhizopus microsporus
to follow the fate of artificially induced endosymbioses. Whereas
Escherichia coli
implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis,
Mycetohabitans rhizoxinica
was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
A study presents an approach to establish and track a new endosymbiotic partnership by implanting bacteria in a non-host fungus and shows that stable inheritance of the implanted bacteria is possible with positive selection. |
doi_str_mv | 10.1038/s41586-024-08010-x |
format | Article |
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1
,
2
. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect
3
–
5
. Here we implant bacteria into the filamentous fungus
Rhizopus microsporus
to follow the fate of artificially induced endosymbioses. Whereas
Escherichia coli
implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis,
Mycetohabitans rhizoxinica
was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
A study presents an approach to establish and track a new endosymbiotic partnership by implanting bacteria in a non-host fungus and shows that stable inheritance of the implanted bacteria is possible with positive selection.</description><identifier>ISSN: 0028-0836</identifier><identifier>ISSN: 1476-4687</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-024-08010-x</identifier><identifier>PMID: 39358514</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/31 ; 14 ; 14/19 ; 14/3 ; 38 ; 38/23 ; 42 ; 42/35 ; 45 ; 631/158/855 ; 631/326/193/2540 ; 631/326/41/547 ; 82 ; Adaptive systems ; Bacteria ; Biological evolution ; Coliforms ; Congeners ; Cytosol ; Cytosol - metabolism ; Cytosol - microbiology ; E coli ; Escherichia coli - physiology ; Evolution ; Evolution & development ; Fungi ; Genetic Fitness ; Humanities and Social Sciences ; Macrolides - chemistry ; Macrolides - metabolism ; Metabolism ; Microscopy ; multidisciplinary ; Mutation ; New combinations ; Phenotype ; Positive selection ; Rare species ; Rhizopus - cytology ; Rhizopus - physiology ; Science ; Science (multidisciplinary) ; Symbiosis - physiology</subject><ispartof>Nature (London), 2024-11, Vol.635 (8038), p.415-422</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>Copyright Nature Publishing Group Nov 14, 2024</rights><rights>The Author(s) 2024 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c356t-c2485b25daba9cd89a167ad749ded8e6623dd56c7f87aa9077d4c77b44c414323</cites><orcidid>0000-0002-3031-8058 ; 0000-0003-1873-8807 ; 0000-0002-0367-337X ; 0000-0003-0965-0950 ; 0000-0002-6011-4910 ; 0000-0003-3065-0314 ; 0000-0002-1326-3761 ; 0000-0003-1275-0629</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-024-08010-x$$EPDF$$P50$$Gspringer$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-024-08010-x$$EHTML$$P50$$Gspringer$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39358514$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Giger, Gabriel H.</creatorcontrib><creatorcontrib>Ernst, Chantal</creatorcontrib><creatorcontrib>Richter, Ingrid</creatorcontrib><creatorcontrib>Gassler, Thomas</creatorcontrib><creatorcontrib>Field, Christopher M.</creatorcontrib><creatorcontrib>Sintsova, Anna</creatorcontrib><creatorcontrib>Kiefer, Patrick</creatorcontrib><creatorcontrib>Gäbelein, Christoph G.</creatorcontrib><creatorcontrib>Guillaume–Gentil, Orane</creatorcontrib><creatorcontrib>Scherlach, Kirstin</creatorcontrib><creatorcontrib>Bortfeld-Miller, Miriam</creatorcontrib><creatorcontrib>Zambelli, Tomaso</creatorcontrib><creatorcontrib>Sunagawa, Shinichi</creatorcontrib><creatorcontrib>Künzler, Markus</creatorcontrib><creatorcontrib>Hertweck, Christian</creatorcontrib><creatorcontrib>Vorholt, Julia A.</creatorcontrib><title>Inducing novel endosymbioses by implanting bacteria in fungi</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification
1
,
2
. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect
3
–
5
. Here we implant bacteria into the filamentous fungus
Rhizopus microsporus
to follow the fate of artificially induced endosymbioses. Whereas
Escherichia coli
implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis,
Mycetohabitans rhizoxinica
was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
A study presents an approach to establish and track a new endosymbiotic partnership by implanting bacteria in a non-host fungus and shows that stable inheritance of the implanted bacteria is possible with positive selection.</description><subject>13/31</subject><subject>14</subject><subject>14/19</subject><subject>14/3</subject><subject>38</subject><subject>38/23</subject><subject>42</subject><subject>42/35</subject><subject>45</subject><subject>631/158/855</subject><subject>631/326/193/2540</subject><subject>631/326/41/547</subject><subject>82</subject><subject>Adaptive systems</subject><subject>Bacteria</subject><subject>Biological evolution</subject><subject>Coliforms</subject><subject>Congeners</subject><subject>Cytosol</subject><subject>Cytosol - metabolism</subject><subject>Cytosol - microbiology</subject><subject>E coli</subject><subject>Escherichia coli - physiology</subject><subject>Evolution</subject><subject>Evolution & development</subject><subject>Fungi</subject><subject>Genetic Fitness</subject><subject>Humanities and Social Sciences</subject><subject>Macrolides - chemistry</subject><subject>Macrolides - metabolism</subject><subject>Metabolism</subject><subject>Microscopy</subject><subject>multidisciplinary</subject><subject>Mutation</subject><subject>New combinations</subject><subject>Phenotype</subject><subject>Positive selection</subject><subject>Rare species</subject><subject>Rhizopus - cytology</subject><subject>Rhizopus - physiology</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Symbiosis - physiology</subject><issn>0028-0836</issn><issn>1476-4687</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><recordid>eNp9kUtLJDEUhYOMaPv4Ay6Ggtm4Kc07KRBExBcIbnQdUkm6jVQlPUlVY_9707bvhau7ON899x4OAAcIHiFI5HGmiEleQ0xrKCGC9fMGmCAqeE25FH_ABEIsi0T4NtjJ-QlCyJCgW2CbNIRJhugEnNwEOxofZlWIC9dVLtiYl33rY3a5apeV7-edDsOKaLUZXPK68qGajmHm98DmVHfZ7b_NXfBweXF_fl3f3l3dnJ_d1oYwPtQGU8lazKxudWOsbDTiQltBG-usdJxjYi3jRkyl0LqBQlhqhGgpNRRRgskuOF37zse2d9a4MCTdqXnyvU5LFbVX35XgH9UsLhRCjENJWXE4fHNI8f_o8qB6n43rSjQXx6wIQphhCSEv6L8f6FMcUyj5CkVwwxCXKwqvKZNizslNP75BUK3aUet2VGlHvbajnsvS3685Plbe6ygAWQO5SGHm0uftX2xfAPilm6c</recordid><startdate>20241114</startdate><enddate>20241114</enddate><creator>Giger, Gabriel H.</creator><creator>Ernst, Chantal</creator><creator>Richter, Ingrid</creator><creator>Gassler, Thomas</creator><creator>Field, Christopher M.</creator><creator>Sintsova, Anna</creator><creator>Kiefer, Patrick</creator><creator>Gäbelein, Christoph G.</creator><creator>Guillaume–Gentil, Orane</creator><creator>Scherlach, Kirstin</creator><creator>Bortfeld-Miller, Miriam</creator><creator>Zambelli, Tomaso</creator><creator>Sunagawa, Shinichi</creator><creator>Künzler, Markus</creator><creator>Hertweck, Christian</creator><creator>Vorholt, Julia A.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>KL.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3031-8058</orcidid><orcidid>https://orcid.org/0000-0003-1873-8807</orcidid><orcidid>https://orcid.org/0000-0002-0367-337X</orcidid><orcidid>https://orcid.org/0000-0003-0965-0950</orcidid><orcidid>https://orcid.org/0000-0002-6011-4910</orcidid><orcidid>https://orcid.org/0000-0003-3065-0314</orcidid><orcidid>https://orcid.org/0000-0002-1326-3761</orcidid><orcidid>https://orcid.org/0000-0003-1275-0629</orcidid></search><sort><creationdate>20241114</creationdate><title>Inducing novel endosymbioses by implanting bacteria in fungi</title><author>Giger, Gabriel H. ; Ernst, Chantal ; Richter, Ingrid ; Gassler, Thomas ; Field, Christopher M. ; Sintsova, Anna ; Kiefer, Patrick ; Gäbelein, Christoph G. ; Guillaume–Gentil, Orane ; Scherlach, Kirstin ; Bortfeld-Miller, Miriam ; Zambelli, Tomaso ; Sunagawa, Shinichi ; Künzler, Markus ; Hertweck, Christian ; Vorholt, Julia A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c356t-c2485b25daba9cd89a167ad749ded8e6623dd56c7f87aa9077d4c77b44c414323</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>13/31</topic><topic>14</topic><topic>14/19</topic><topic>14/3</topic><topic>38</topic><topic>38/23</topic><topic>42</topic><topic>42/35</topic><topic>45</topic><topic>631/158/855</topic><topic>631/326/193/2540</topic><topic>631/326/41/547</topic><topic>82</topic><topic>Adaptive systems</topic><topic>Bacteria</topic><topic>Biological evolution</topic><topic>Coliforms</topic><topic>Congeners</topic><topic>Cytosol</topic><topic>Cytosol - metabolism</topic><topic>Cytosol - microbiology</topic><topic>E coli</topic><topic>Escherichia coli - physiology</topic><topic>Evolution</topic><topic>Evolution & development</topic><topic>Fungi</topic><topic>Genetic Fitness</topic><topic>Humanities and Social Sciences</topic><topic>Macrolides - chemistry</topic><topic>Macrolides - metabolism</topic><topic>Metabolism</topic><topic>Microscopy</topic><topic>multidisciplinary</topic><topic>Mutation</topic><topic>New combinations</topic><topic>Phenotype</topic><topic>Positive selection</topic><topic>Rare species</topic><topic>Rhizopus - cytology</topic><topic>Rhizopus - physiology</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Symbiosis - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Giger, Gabriel H.</creatorcontrib><creatorcontrib>Ernst, Chantal</creatorcontrib><creatorcontrib>Richter, Ingrid</creatorcontrib><creatorcontrib>Gassler, Thomas</creatorcontrib><creatorcontrib>Field, Christopher M.</creatorcontrib><creatorcontrib>Sintsova, Anna</creatorcontrib><creatorcontrib>Kiefer, Patrick</creatorcontrib><creatorcontrib>Gäbelein, Christoph G.</creatorcontrib><creatorcontrib>Guillaume–Gentil, Orane</creatorcontrib><creatorcontrib>Scherlach, Kirstin</creatorcontrib><creatorcontrib>Bortfeld-Miller, Miriam</creatorcontrib><creatorcontrib>Zambelli, Tomaso</creatorcontrib><creatorcontrib>Sunagawa, Shinichi</creatorcontrib><creatorcontrib>Künzler, Markus</creatorcontrib><creatorcontrib>Hertweck, Christian</creatorcontrib><creatorcontrib>Vorholt, Julia A.</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Giger, Gabriel H.</au><au>Ernst, Chantal</au><au>Richter, Ingrid</au><au>Gassler, Thomas</au><au>Field, Christopher M.</au><au>Sintsova, Anna</au><au>Kiefer, Patrick</au><au>Gäbelein, Christoph G.</au><au>Guillaume–Gentil, Orane</au><au>Scherlach, Kirstin</au><au>Bortfeld-Miller, Miriam</au><au>Zambelli, Tomaso</au><au>Sunagawa, Shinichi</au><au>Künzler, Markus</au><au>Hertweck, Christian</au><au>Vorholt, Julia A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Inducing novel endosymbioses by implanting bacteria in fungi</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2024-11-14</date><risdate>2024</risdate><volume>635</volume><issue>8038</issue><spage>415</spage><epage>422</epage><pages>415-422</pages><issn>0028-0836</issn><issn>1476-4687</issn><eissn>1476-4687</eissn><abstract>Endosymbioses have profoundly impacted the evolution of life and continue to shape the ecology of a wide range of species. They give rise to new combinations of biochemical capabilities that promote innovation and diversification
1
,
2
. Despite the many examples of known endosymbioses across the tree of life, their de novo emergence is rare and challenging to uncover in retrospect
3
–
5
. Here we implant bacteria into the filamentous fungus
Rhizopus microsporus
to follow the fate of artificially induced endosymbioses. Whereas
Escherichia coli
implanted into the cytosol induced septum formation, effectively halting endosymbiogenesis,
Mycetohabitans rhizoxinica
was transmitted vertically to the progeny at a low frequency. Continuous positive selection on endosymbiosis mitigated initial fitness constraints by several orders of magnitude upon adaptive evolution. Phenotypic changes were underscored by the accumulation of mutations in the host as the system stabilized. The bacterium produced rhizoxin congeners in its new host, demonstrating the transfer of a metabolic function through induced endosymbiosis. Single-cell implantation thus provides a powerful experimental approach to study critical events at the onset of endosymbiogenesis and opens opportunities for synthetic approaches towards designing endosymbioses with desired traits.
A study presents an approach to establish and track a new endosymbiotic partnership by implanting bacteria in a non-host fungus and shows that stable inheritance of the implanted bacteria is possible with positive selection.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>39358514</pmid><doi>10.1038/s41586-024-08010-x</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-3031-8058</orcidid><orcidid>https://orcid.org/0000-0003-1873-8807</orcidid><orcidid>https://orcid.org/0000-0002-0367-337X</orcidid><orcidid>https://orcid.org/0000-0003-0965-0950</orcidid><orcidid>https://orcid.org/0000-0002-6011-4910</orcidid><orcidid>https://orcid.org/0000-0003-3065-0314</orcidid><orcidid>https://orcid.org/0000-0002-1326-3761</orcidid><orcidid>https://orcid.org/0000-0003-1275-0629</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 13/31 14 14/19 14/3 38 38/23 42 42/35 45 631/158/855 631/326/193/2540 631/326/41/547 82 Adaptive systems Bacteria Biological evolution Coliforms Congeners Cytosol Cytosol - metabolism Cytosol - microbiology E coli Escherichia coli - physiology Evolution Evolution & development Fungi Genetic Fitness Humanities and Social Sciences Macrolides - chemistry Macrolides - metabolism Metabolism Microscopy multidisciplinary Mutation New combinations Phenotype Positive selection Rare species Rhizopus - cytology Rhizopus - physiology Science Science (multidisciplinary) Symbiosis - physiology |
title | Inducing novel endosymbioses by implanting bacteria in fungi |
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