Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae
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...
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Published in | mSystems Vol. 6; no. 6; p. e0083521 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
American Society for Microbiology
21.12.2021
|
Subjects | |
Online Access | Get full text |
ISSN | 2379-5077 2379-5077 |
DOI | 10.1128/mSystems.00835-21 |
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Abstract | 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.
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. |
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AbstractList | 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.
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. 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. 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. 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. 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. 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 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'- -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. 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. 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.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. |
Author | Bowen, Benjamin Golini, Amber Thelen, Michael Stuart, Rhona K. Mayali, Xavier Brisson, Vanessa Northen, Trent R. |
Author_xml | – sequence: 1 givenname: Vanessa surname: Brisson fullname: Brisson, Vanessa organization: Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA – sequence: 2 givenname: Xavier orcidid: 0000-0002-2170-0773 surname: Mayali fullname: Mayali, Xavier organization: Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA – sequence: 3 givenname: Benjamin surname: Bowen fullname: Bowen, Benjamin organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA – sequence: 4 givenname: Amber surname: Golini fullname: Golini, Amber organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA – sequence: 5 givenname: Michael orcidid: 0000-0002-2479-5480 surname: Thelen fullname: Thelen, Michael organization: Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA – sequence: 6 givenname: Rhona K. surname: Stuart fullname: Stuart, Rhona K. organization: Physical and Life Sciences Directorate, Lawrence Livermore National Laboratory, Livermore, California, USA – sequence: 7 givenname: Trent R. surname: Northen fullname: Northen, Trent R. organization: Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, California, USA, The DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Berkeley, California, USA |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34726483$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1842430$$D View this record in Osti.gov |
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ContentType | Journal Article |
CorporateAuthor | Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States) Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States) |
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Keywords | lumichrome Microchloropsis salina Chlamydomonas reinhardtii Phaeodactylum tricornutum microalgae Desmodesmus effector metabolites Chlamydononas reinhardtii exometabolome |
Language | English |
License | This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AC52-07NA27344; AC02-05CH11231 LLNL-JRNL-823908 USDOE Office of Science (SC), Biological and Environmental Research (BER) Citation Brisson V, Mayali X, Bowen B, Golini A, Thelen M, Stuart RK, Northen TR. 2021. Identification of effector metabolites using exometabolite profiling of diverse microalgae. mSystems 6:e00835-21. https://doi.org/10.1128/mSystems.00835-21. |
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PublicationDate | 2021-Dec-21 |
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PublicationPlace | United States |
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PublicationTitle | mSystems |
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Publisher | American Society for Microbiology |
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Snippet | 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... Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an untargeted... ABSTRACT Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an... |
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SubjectTerms | BASIC BIOLOGICAL SCIENCES biological and medical sciences biomass Chlamydomonas reinhardtii Desmodesmus effector metabolites energy Environmental Microbiology environmental sciences exometabolome lumichrome microalgae Research Article |
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Title | Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae |
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