Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling
ABSTRACT The importance of defensive symbioses, whereby microbes protect hosts through the production of specific compounds, is becoming increasingly evident. Although defining the partners in these associations has become easier, assigning function to these relationships often presents a significan...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2019-10-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.02376-19 |
| _version_ | 1798032254441619456 |
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| author | Allison H. Kerwin Samantha M. Gromek Andrea M. Suria Robert M. Samples Dister J. Deoss Kerry O’Donnell Salvatore Frasca Deanna A. Sutton Nathan P. Wiederhold Marcy J. Balunas Spencer V. Nyholm |
| author_facet | Allison H. Kerwin Samantha M. Gromek Andrea M. Suria Robert M. Samples Dister J. Deoss Kerry O’Donnell Salvatore Frasca Deanna A. Sutton Nathan P. Wiederhold Marcy J. Balunas Spencer V. Nyholm |
| author_sort | Allison H. Kerwin |
| collection | DOAJ |
| description | ABSTRACT The importance of defensive symbioses, whereby microbes protect hosts through the production of specific compounds, is becoming increasingly evident. Although defining the partners in these associations has become easier, assigning function to these relationships often presents a significant challenge. Here, we describe a functional role for a bacterial consortium in a female reproductive organ in the Hawaiian bobtail squid, Euprymna scolopes. Bacteria from the accessory nidamental gland (ANG) are deposited into the egg jelly coat (JC), where they are hypothesized to play a defensive role during embryogenesis. Eggs treated with an antibiotic cocktail developed a microbial biomass primarily composed of the pathogenic fungus Fusarium keratoplasticum that infiltrated the JC, resulting in severely reduced hatch rates. Experimental manipulation of the eggs demonstrated that the JC was protective against this fungal fouling. A large proportion of the bacterial strains isolated from the ANG or JC inhibited F. keratoplasticum in culture (87.5%), while a similar proportion of extracts from these strains also exhibited antifungal activity against F. keratoplasticum and/or the human-pathogenic yeast Candida albicans (72.7%). Mass spectral network analyses of active extracts from bacterial isolates and egg clutches revealed compounds that may be involved in preventing microbial overgrowth. Several secondary metabolites were identified from ANG/JC bacteria and egg clutches, including the known antimicrobial lincomycin as well as a suite of glycerophosphocholines and mycinamicin-like compounds. These results shed light on a widely distributed but poorly understood symbiosis in cephalopods and offer a new source for exploring bacterial secondary metabolites with antimicrobial activity. IMPORTANCE Organisms must have strategies to ensure successful reproduction. Some animals that deposit eggs protect their embryos from fouling/disease with the help of microorganisms. Although beneficial bacteria are hypothesized to contribute to egg defense in some organisms, the mechanisms of this protection remain largely unknown, with the exception of a few recently described systems. Using both experimental and analytical approaches, we demonstrate that symbiotic bacteria associated with a cephalopod reproductive gland and eggs inhibit fungi. Chemical analyses suggest that these bacteria produce antimicrobial compounds that may prevent overgrowth from fungi and other microorganisms. Given the distribution of these symbiotic glands among many cephalopods, similar defensive relationships may be more common in aquatic environments than previously realized. Such defensive symbioses may also be a rich source for the discovery of new antimicrobial compounds. |
| first_indexed | 2024-04-11T20:09:50Z |
| format | Article |
| id | doaj.art-f00a79019fb241a99914de03e5a6d035 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-04-11T20:09:50Z |
| publishDate | 2019-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-f00a79019fb241a99914de03e5a6d0352022-12-22T04:05:10ZengAmerican Society for MicrobiologymBio2150-75112019-10-0110510.1128/mBio.02376-19Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal FoulingAllison H. Kerwin0Samantha M. Gromek1Andrea M. Suria2Robert M. Samples3Dister J. Deoss4Kerry O’Donnell5Salvatore Frasca6Deanna A. Sutton7Nathan P. Wiederhold8Marcy J. Balunas9Spencer V. Nyholm10Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USADivision of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, Connecticut, USADepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USADivision of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, Connecticut, USADepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USAMycotoxin Prevention and Applied Microbiology Research Unit, National Center for Agricultural Utilization Research, Agricultural Research Service, U.S. Department of Agriculture, Peoria, Illinois, USADepartment of Comparative, Diagnostic, and Population Medicine, College of Veterinary Medicine, University of Florida, Gainesville, Florida, USADepartment of Pathology and Laboratory Medicine, Fungus Testing Laboratory, University of Texas Health Science Center, San Antonio, Texas, USADepartment of Pathology and Laboratory Medicine, Fungus Testing Laboratory, University of Texas Health Science Center, San Antonio, Texas, USADivision of Medicinal Chemistry, Department of Pharmaceutical Sciences, University of Connecticut, Storrs, Connecticut, USADepartment of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USAABSTRACT The importance of defensive symbioses, whereby microbes protect hosts through the production of specific compounds, is becoming increasingly evident. Although defining the partners in these associations has become easier, assigning function to these relationships often presents a significant challenge. Here, we describe a functional role for a bacterial consortium in a female reproductive organ in the Hawaiian bobtail squid, Euprymna scolopes. Bacteria from the accessory nidamental gland (ANG) are deposited into the egg jelly coat (JC), where they are hypothesized to play a defensive role during embryogenesis. Eggs treated with an antibiotic cocktail developed a microbial biomass primarily composed of the pathogenic fungus Fusarium keratoplasticum that infiltrated the JC, resulting in severely reduced hatch rates. Experimental manipulation of the eggs demonstrated that the JC was protective against this fungal fouling. A large proportion of the bacterial strains isolated from the ANG or JC inhibited F. keratoplasticum in culture (87.5%), while a similar proportion of extracts from these strains also exhibited antifungal activity against F. keratoplasticum and/or the human-pathogenic yeast Candida albicans (72.7%). Mass spectral network analyses of active extracts from bacterial isolates and egg clutches revealed compounds that may be involved in preventing microbial overgrowth. Several secondary metabolites were identified from ANG/JC bacteria and egg clutches, including the known antimicrobial lincomycin as well as a suite of glycerophosphocholines and mycinamicin-like compounds. These results shed light on a widely distributed but poorly understood symbiosis in cephalopods and offer a new source for exploring bacterial secondary metabolites with antimicrobial activity. IMPORTANCE Organisms must have strategies to ensure successful reproduction. Some animals that deposit eggs protect their embryos from fouling/disease with the help of microorganisms. Although beneficial bacteria are hypothesized to contribute to egg defense in some organisms, the mechanisms of this protection remain largely unknown, with the exception of a few recently described systems. Using both experimental and analytical approaches, we demonstrate that symbiotic bacteria associated with a cephalopod reproductive gland and eggs inhibit fungi. Chemical analyses suggest that these bacteria produce antimicrobial compounds that may prevent overgrowth from fungi and other microorganisms. Given the distribution of these symbiotic glands among many cephalopods, similar defensive relationships may be more common in aquatic environments than previously realized. Such defensive symbioses may also be a rich source for the discovery of new antimicrobial compounds.https://journals.asm.org/doi/10.1128/mBio.02376-19host-microbe symbiosesEuprymna scolopeschemical defenseinteraction-driven molecular networkingdefensive symbiosis |
| spellingShingle | Allison H. Kerwin Samantha M. Gromek Andrea M. Suria Robert M. Samples Dister J. Deoss Kerry O’Donnell Salvatore Frasca Deanna A. Sutton Nathan P. Wiederhold Marcy J. Balunas Spencer V. Nyholm Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling mBio host-microbe symbioses Euprymna scolopes chemical defense interaction-driven molecular networking defensive symbiosis |
| title | Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling |
| title_full | Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling |
| title_fullStr | Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling |
| title_full_unstemmed | Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling |
| title_short | Shielding the Next Generation: Symbiotic Bacteria from a Reproductive Organ Protect Bobtail Squid Eggs from Fungal Fouling |
| title_sort | shielding the next generation symbiotic bacteria from a reproductive organ protect bobtail squid eggs from fungal fouling |
| topic | host-microbe symbioses Euprymna scolopes chemical defense interaction-driven molecular networking defensive symbiosis |
| url | https://journals.asm.org/doi/10.1128/mBio.02376-19 |
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