Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae
ABSTRACT Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an untargeted metabolomic analysis of nonpolar exometabolites exuded from four phylogenetically and ecologically diverse eukaryotic microalgal strains g...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2021-12-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00835-21 |
| _version_ | 1818979327261278208 |
|---|---|
| author | Vanessa Brisson Xavier Mayali Benjamin Bowen Amber Golini Michael Thelen Rhona K. Stuart Trent R. Northen |
| author_facet | Vanessa Brisson Xavier Mayali Benjamin Bowen Amber Golini Michael Thelen Rhona K. Stuart Trent R. Northen |
| author_sort | Vanessa Brisson |
| collection | DOAJ |
| description | ABSTRACT Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an untargeted metabolomic analysis of nonpolar exometabolites exuded from four phylogenetically and ecologically diverse eukaryotic microalgal strains grown in the laboratory, freshwater Chlamydomonas reinhardtii, brackish Desmodesmus sp., marine Phaeodactylum tricornutum, and marine Microchloropsis salina, to identify released metabolites based on relative enrichment in the exometabolomes compared to cell pellet metabolomes. Exudates from the different taxa were distinct, but we did not observe clear phylogenetic patterns. We used feature-based molecular networking to explore the identities of these metabolites, revealing several distinct di- and tripeptides secreted by each of the algae, lumichrome, a compound that is known to be involved in plant growth and bacterial quorum sensing, and novel prostaglandin-like compounds. We further investigated the impacts of exogenous additions of eight compounds selected based on exometabolome enrichment on algal growth. Of these compounds, five (lumichrome, 5′-S-methyl-5′-thioadenosine, 17-phenyl trinor prostaglandin A2, dodecanedioic acid, and aleuritic acid) impacted growth in at least one of the algal cultures. Two of these compounds (dodecanedioic acid and aleuritic acid) produced contrasting results, increasing growth in some algae and decreasing growth in others. Together, our results reveal new groups of microalgal exometabolites, some of which could alter algal growth when provided exogenously, suggesting potential roles in allelopathy and algal interactions. IMPORTANCE Microalgae are responsible for nearly half of primary production on earth and play an important role in global biogeochemical cycling as well as in a range of industrial applications. Algal exometabolites are important mediators of algal-algal and algal-bacterial interactions that ultimately affect algal growth and physiology. In this study, we characterize exometabolomes across marine and freshwater algae to gain insights into the diverse metabolites they release into their environments (“exudates”). We observe that while phylogeny can play a role in exometabolome content, environmental conditions or habitat origin (freshwater versus marine) are also important. We also find that several of these compounds can influence algal growth (as measured by chlorophyll production) when provided exogenously, highlighting the importance of characterization of these novel compounds and their role in microalgal ecophysiology. |
| first_indexed | 2024-12-20T16:57:46Z |
| format | Article |
| id | doaj.art-ee163451f1cf463e947fca391bbaad35 |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-20T16:57:46Z |
| publishDate | 2021-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-ee163451f1cf463e947fca391bbaad352022-12-21T19:32:41ZengAmerican Society for MicrobiologymSystems2379-50772021-12-016610.1128/mSystems.00835-21Identification of Effector Metabolites Using Exometabolite Profiling of Diverse MicroalgaeVanessa Brisson0Xavier Mayali1Benjamin Bowen2Amber Golini3Michael Thelen4Rhona K. Stuart5Trent R. Northen6Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USAPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USAEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USAEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USAPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USAPhysical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USAEnvironmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USAABSTRACT Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an untargeted metabolomic analysis of nonpolar exometabolites exuded from four phylogenetically and ecologically diverse eukaryotic microalgal strains grown in the laboratory, freshwater Chlamydomonas reinhardtii, brackish Desmodesmus sp., marine Phaeodactylum tricornutum, and marine Microchloropsis salina, to identify released metabolites based on relative enrichment in the exometabolomes compared to cell pellet metabolomes. Exudates from the different taxa were distinct, but we did not observe clear phylogenetic patterns. We used feature-based molecular networking to explore the identities of these metabolites, revealing several distinct di- and tripeptides secreted by each of the algae, lumichrome, a compound that is known to be involved in plant growth and bacterial quorum sensing, and novel prostaglandin-like compounds. We further investigated the impacts of exogenous additions of eight compounds selected based on exometabolome enrichment on algal growth. Of these compounds, five (lumichrome, 5′-S-methyl-5′-thioadenosine, 17-phenyl trinor prostaglandin A2, dodecanedioic acid, and aleuritic acid) impacted growth in at least one of the algal cultures. Two of these compounds (dodecanedioic acid and aleuritic acid) produced contrasting results, increasing growth in some algae and decreasing growth in others. Together, our results reveal new groups of microalgal exometabolites, some of which could alter algal growth when provided exogenously, suggesting potential roles in allelopathy and algal interactions. IMPORTANCE Microalgae are responsible for nearly half of primary production on earth and play an important role in global biogeochemical cycling as well as in a range of industrial applications. Algal exometabolites are important mediators of algal-algal and algal-bacterial interactions that ultimately affect algal growth and physiology. In this study, we characterize exometabolomes across marine and freshwater algae to gain insights into the diverse metabolites they release into their environments (“exudates”). We observe that while phylogeny can play a role in exometabolome content, environmental conditions or habitat origin (freshwater versus marine) are also important. We also find that several of these compounds can influence algal growth (as measured by chlorophyll production) when provided exogenously, highlighting the importance of characterization of these novel compounds and their role in microalgal ecophysiology.https://journals.asm.org/doi/10.1128/mSystems.00835-21microalgaeexometabolomeeffector metaboliteslumichromeChlamydomonas reinhardtiiDesmodesmus |
| spellingShingle | Vanessa Brisson Xavier Mayali Benjamin Bowen Amber Golini Michael Thelen Rhona K. Stuart Trent R. Northen Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae mSystems microalgae exometabolome effector metabolites lumichrome Chlamydomonas reinhardtii Desmodesmus |
| title | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
| title_full | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
| title_fullStr | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
| title_full_unstemmed | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
| title_short | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
| title_sort | identification of effector metabolites using exometabolite profiling of diverse microalgae |
| topic | microalgae exometabolome effector metabolites lumichrome Chlamydomonas reinhardtii Desmodesmus |
| url | https://journals.asm.org/doi/10.1128/mSystems.00835-21 |
| work_keys_str_mv | AT vanessabrisson identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT xaviermayali identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT benjaminbowen identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT ambergolini identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT michaelthelen identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT rhonakstuart identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae AT trentrnorthen identificationofeffectormetabolitesusingexometaboliteprofilingofdiversemicroalgae |