Costs and Limitations of Marine Synechococcus Blue-Green Chromatic Acclimation
Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing chromatic acclimation using a fluorescence-based calculation of light use efficiency. Using laboratory cultures and artificial light environmen...
Saved in:
Published in: | Frontiers in Marine Science Vol. 8 |
---|---|
Main Authors: | , , , |
Format: | Journal Article |
Language: | English |
Published: |
Frontiers Media S.A
03-09-2021
|
Subjects: | |
Online Access: | Get full text |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
Abstract | Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing chromatic acclimation using a fluorescence-based calculation of light use efficiency. Using laboratory cultures and artificial light environments, we show that the delayed response to acclimation known to occur in marine
Synechococcus
acclimating strains (generalists) in green light do not reduce light use efficiency in green light, but that only one generalist, RCC307, with a much smaller range of acclimation, had higher light use efficiency than blue and green light specialist strains. Generalists with a wider acclimation range either had the same or >30% lower light use efficiencies in blue and green light environments. From this work, we propose that advantages from CA4 may not be geared at direct competition with other
Synechococcus
specialists with fixed pigment types, but may serve to expand the ecological range of
Synechococcus
in spectral competition with other genera. As all eight
Synechococcus
strains tested had higher light use efficiency in green light, regardless of a fixed or flexible light harvesting strategy, we add evidence to the suitability of the
Synechococcus
genus to greener ocean niches, whether stable, or variable. |
---|---|
AbstractList | Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing chromatic acclimation using a fluorescence-based calculation of light use efficiency. Using laboratory cultures and artificial light environments, we show that the delayed response to acclimation known to occur in marine Synechococcus acclimating strains (generalists) in green light do not reduce light use efficiency in green light, but that only one generalist, RCC307, with a much smaller range of acclimation, had higher light use efficiency than blue and green light specialist strains. Generalists with a wider acclimation range either had the same or >30% lower light use efficiencies in blue and green light environments. From this work, we propose that advantages from CA4 may not be geared at direct competition with other Synechococcus specialists with fixed pigment types, but may serve to expand the ecological range of Synechococcus in spectral competition with other genera. As all eight Synechococcus strains tested had higher light use efficiency in green light, regardless of a fixed or flexible light harvesting strategy, we add evidence to the suitability of the Synechococcus genus to greener ocean niches, whether stable, or variable. Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing chromatic acclimation using a fluorescence-based calculation of light use efficiency. Using laboratory cultures and artificial light environments, we show that the delayed response to acclimation known to occur in marine Synechococcus acclimating strains (generalists) in green light do not reduce light use efficiency in green light, but that only one generalist, RCC307, with a much smaller range of acclimation, had higher light use efficiency than blue and green light specialist strains. Generalists with a wider acclimation range either had the same or >30% lower light use efficiencies in blue and green light environments. From this work, we propose that advantages from CA4 may not be geared at direct competition with other Synechococcus specialists with fixed pigment types, but may serve to expand the ecological range of Synechococcus in spectral competition with other genera. As all eight Synechococcus strains tested had higher light use efficiency in green light, regardless of a fixed or flexible light harvesting strategy, we add evidence to the suitability of the Synechococcus genus to greener ocean niches, whether stable, or variable. |
Author | Mackey, Katherine R. M. Lovindeer, Raisha Medina, Hannah Abbott, Lawrence |
Author_xml | – sequence: 1 givenname: Raisha surname: Lovindeer fullname: Lovindeer, Raisha – sequence: 2 givenname: Lawrence surname: Abbott fullname: Abbott, Lawrence – sequence: 3 givenname: Hannah surname: Medina fullname: Medina, Hannah – sequence: 4 givenname: Katherine R. M. surname: Mackey fullname: Mackey, Katherine R. M. |
BookMark | eNpNkM1OwzAMgCMEEmPsAbj1BTqSOM3PcUwwJg04AOcozQ_r1DYo6Q57e7oNISRLtiz7s_XdoMs-9h6hO4LnAFLdh86kPKeYkjmXSil5gSaUKl4KwarLf_U1muW8wxgTYLhiaoJelzEPuTC9KzZN1wxmaGKfixiKF5Oa3hfvh97bbbTR2n0uHtq9L1fJ-75YblPsxnFbLKxtm-60eYuugmmzn_3mKfp8evxYPpebt9V6udiUFio2lKSuJPGUS2MUcwA1cQJzgABV4MB5zSE4LiWtmWCOByGpVRRoPYZlXMIUrc9cF81Of6fxfDroaBp9asT0pU0af2u9HjcEU5ULwC0jdPSFHShma6-UqIQZWeTMsinmnHz44xGsj371ya8--tVnv_ADR-Vvvw |
CitedBy_id | crossref_primary_10_3390_su14159508 crossref_primary_10_1029_2021JC017434 crossref_primary_10_3389_fmicb_2024_1349322 |
Cites_doi | 10.1016/0198-0149(87)90001-X 10.1007/s11120-019-00630-z 10.1073/pnas.1717069115 10.1016/j.pbi.2017.03.009 10.1016/j.algal.2016.02.005 10.1016/j.rse.2011.10.001 10.1016/j.seares.2005.04.006 10.1038/s41559-020-01330-x 10.1073/pnas.1211777109 10.1073/pnas.2024583118 10.1023/A:1005807221560 10.1093/jxb/erw206 10.1128/mBio.02130-15 10.1007/s00248-017-1021-z 10.1016/S0169-5347(97)01274-3 10.1186/gb-2007-8-12-r259 10.1073/pnas.1810491116 10.1128/AEM.67.2.991-994.2001 10.1093/oxfordjournals.pcp.a078833 10.1371/journal.pone.0001341 10.3354/meps07830 10.1016/S0967-0645(00)00166-1 10.1371/journal.pone.0084459 10.1099/13500872-142-5-1255 10.1073/pnas.1306332110 10.1128/JB.187.5.1685-1694.2005 10.1046/j.1365-2958.2003.03853.x 10.1111/1574-6941.12285 10.1146/annurev-micro-020518-115738 10.1073/pnas.1600625113 10.3354/ame035017 10.1007/s11120-018-0561-5 10.1086/591680 10.1111/1462-2920.13744 10.1038/s41579-018-0110-4 10.1073/pnas.2019715118 10.1128/JB.188.9.3345-3356.2006 10.3389/fmicb.2017.00243 10.3389/fmicb.2017.01254 10.1038/s41396-018-0287-6 |
ContentType | Journal Article |
DBID | AAYXX CITATION DOA |
DOI | 10.3389/fmars.2021.689998 |
DatabaseName | CrossRef Directory of Open Access Journals |
DatabaseTitle | CrossRef |
DatabaseTitleList | CrossRef |
Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals url: http://www.doaj.org/ sourceTypes: Open Website |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Oceanography |
EISSN | 2296-7745 |
ExternalDocumentID | oai_doaj_org_article_2bc7495df36c4123890d394cbe99757a 10_3389_fmars_2021_689998 |
GroupedDBID | 5VS 88I 8FE 8FH 9T4 AAFWJ AAYXX ABUWG ACGFS ACXDI ADBBV AFKRA AFPKN ALMA_UNASSIGNED_HOLDINGS AZQEC BBNVY BCNDV BENPR BHPHI BKSAR BPHCQ CCPQU CITATION DWQXO FRP GNUQQ GROUPED_DOAJ HCIFZ IAO IEA IGS KQ8 LK8 M2P M7P M~E OK1 PCBAR PIMPY PQQKQ PROAC |
ID | FETCH-LOGICAL-c354t-1b581e268aa94d33b1d70633f35f6366b63fd6882b474d6f782c9232b32bc4683 |
IEDL.DBID | DOA |
ISSN | 2296-7745 |
IngestDate | Tue Oct 22 14:57:49 EDT 2024 Thu Nov 21 20:54:29 EST 2024 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
Language | English |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c354t-1b581e268aa94d33b1d70633f35f6366b63fd6882b474d6f782c9232b32bc4683 |
OpenAccessLink | https://doaj.org/article/2bc7495df36c4123890d394cbe99757a |
ParticipantIDs | doaj_primary_oai_doaj_org_article_2bc7495df36c4123890d394cbe99757a crossref_primary_10_3389_fmars_2021_689998 |
PublicationCentury | 2000 |
PublicationDate | 2021-09-03 |
PublicationDateYYYYMMDD | 2021-09-03 |
PublicationDate_xml | – month: 09 year: 2021 text: 2021-09-03 day: 03 |
PublicationDecade | 2020 |
PublicationTitle | Frontiers in Marine Science |
PublicationYear | 2021 |
Publisher | Frontiers Media S.A |
Publisher_xml | – name: Frontiers Media S.A |
References | Gutu (B9) 2013; 110 Sanfilippo (B26) 2016; 113 Holtrop (B10) 2020; 5 Six (B30) 2004; 35 Xia (B39) 2017; 8 Terauchi (B36) 2004; 51 Luimstra (B15) 2019; 141 Montgomery (B19) 2016; 67 Montgomery (B20) 2017; 37 Sanfilippo (B24); 73 Stambler (B33) 2005; 54 Xia (B40) 2018; 75 Grébert (B7) 2021; 118 Palenik (B23) 2001; 67 Shukla (B28) 2012; 109 Mahmoud (B18) 2017; 8 Everroad (B5) 2006; 188 Six (B31); 8 Grossman (B8) 1997; 53 Humily (B12) 2013; 8 Sanfilippo (B25); 116 Mackey (B17) 2017; 19 Schreiber (B27) 1995; 36 Humily (B11) 2014; 88 Moore (B21) 2012; 117 Agostoni (B1) 2016; 15 Stomp (B34) 2008; 172 Suggett (B35) 2009; 376 Wiltbank (B37) 2016; 7 Wiltbank (B38) 2019; 17 Kent (B14) 2019; 13 Campbell (B2) 1996; 142 Kana (B13) 1987; 34 Nagae (B22) 2021; 118 Six (B29); 2 DuRand (B4) 2001; 48 Luimstra (B16) 2018; 138 DeWitt (B3) 1998; 13 Grébert (B6) 2018; 115 Six (B32) 2005; 187 |
References_xml | – volume: 34 start-page: 479 year: 1987 ident: B13 article-title: Effect of irradiances up to 2000 uE m-2 s-l on marine Synechococcus WH7803I. growth, pigmentation, and cell composition. publication-title: Deep Sea Res. doi: 10.1016/0198-0149(87)90001-X contributor: fullname: Kana – volume: 141 start-page: 291 year: 2019 ident: B15 article-title: Exploring the low photosynthetic efficiency of cyanobacteria in blue light using a mutant lacking phycobilisomes. publication-title: Photosy. Res. doi: 10.1007/s11120-019-00630-z contributor: fullname: Luimstra – volume: 115 start-page: E2010 year: 2018 ident: B6 article-title: Light color acclimation is a key process in the global ocean distribution of Synechococcus cyanobacteria. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1717069115 contributor: fullname: Grébert – volume: 37 start-page: 18 year: 2017 ident: B20 article-title: Seeing new light: recent insights into the occurrence and regulation of chromatic acclimation in cyanobacteria. publication-title: Curr. Opin. Plant Biol. doi: 10.1016/j.pbi.2017.03.009 contributor: fullname: Montgomery – volume: 15 start-page: 110 year: 2016 ident: B1 article-title: Competition-based phenotyping reveals a fitness cost for maintaining phycobilisomes under fluctuating light in the cyanobacterium Fremyella diplosiphon. publication-title: Algal Res. doi: 10.1016/j.algal.2016.02.005 contributor: fullname: Agostoni – volume: 117 start-page: 249 year: 2012 ident: B21 article-title: Detection of coccolithophore blooms in ocean color satellite imagery: a generalized approach for use with multiple sensors. publication-title: Remote Sensing Environ. doi: 10.1016/j.rse.2011.10.001 contributor: fullname: Moore – volume: 54 start-page: 186 year: 2005 ident: B33 article-title: Bio-optical properties of the northern red sea and the gulf of eilat (Aqaba) during winter 1999. publication-title: J. Sea Res. doi: 10.1016/j.seares.2005.04.006 contributor: fullname: Stambler – volume: 5 start-page: 55 year: 2020 ident: B10 article-title: Vibrational modes of water predict spectral niches for photosynthesis in lakes and oceans. publication-title: Nat. Ecol. Evolu. doi: 10.1038/s41559-020-01330-x contributor: fullname: Holtrop – volume: 109 start-page: 20136 year: 2012 ident: B28 article-title: Phycoerythrin-specific bilin lyase-isomerase controls blue-green chromatic acclimation in marine Synechococcus. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1211777109 contributor: fullname: Shukla – volume: 118 year: 2021 ident: B22 article-title: Structural basis of the protochromic green/red photocycle of the chromatic acclimation sensor RcaE. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.2024583118 contributor: fullname: Nagae – volume: 53 start-page: 95 year: 1997 ident: B8 article-title: Phosphorelay control of phycobilisome biogenesis during complementary chromatic adaptation. publication-title: Photosy. Res. doi: 10.1023/A:1005807221560 contributor: fullname: Grossman – volume: 67 start-page: 4079 year: 2016 ident: B19 article-title: Mechanisms and fitness implications of photomorphogenesis during chromatic acclimation in cyanobacteria. publication-title: J. Exp. Bot. doi: 10.1093/jxb/erw206 contributor: fullname: Montgomery – volume: 7 year: 2016 ident: B37 article-title: Two Cyanobacterial Photoreceptors regulate photosynthetic light harvesting by sensing teal, green, yellow, and red light. publication-title: MBio doi: 10.1128/mBio.02130-15 contributor: fullname: Wiltbank – volume: 75 start-page: 10 year: 2018 ident: B40 article-title: Variation of Synechococcus pigment genetic diversity along two turbidity gradients in the china seas. publication-title: Microbial. Ecol. doi: 10.1007/s00248-017-1021-z contributor: fullname: Xia – volume: 13 start-page: 77 year: 1998 ident: B3 article-title: Costs and limits of phenotypic plasticity. publication-title: Trends Ecol. Evolu. doi: 10.1016/S0169-5347(97)01274-3 contributor: fullname: DeWitt – volume: 8 ident: B31 article-title: Diversity and evolution of phycobilisomes in marine Synechococcus spp.: a comparative genomics study. publication-title: Genome Biol. doi: 10.1186/gb-2007-8-12-r259 contributor: fullname: Six – volume: 116 start-page: 6457 ident: B25 article-title: Interplay between differentially expressed enzymes contributes to light color acclimation in marine Synechococcus. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1810491116 contributor: fullname: Sanfilippo – volume: 67 start-page: 991 year: 2001 ident: B23 article-title: Chromatic adaptation in marine Synechococcus strains. publication-title: Appl. Environ. Microbiol. doi: 10.1128/AEM.67.2.991-994.2001 contributor: fullname: Palenik – volume: 36 start-page: 873 year: 1995 ident: B27 article-title: Quenching analysis of chlorophyll fluorescence by the saturation pulse method: particular aspects relating to the study of eukaryotic algae and cyanobacteria. publication-title: Plant Cell Physiol. doi: 10.1093/oxfordjournals.pcp.a078833 contributor: fullname: Schreiber – volume: 2 ident: B29 article-title: Light variability illuminates niche-partitioning among marine Picocyanobacteria. publication-title: PLoS One doi: 10.1371/journal.pone.0001341 contributor: fullname: Six – volume: 376 start-page: 1 year: 2009 ident: B35 article-title: Interpretation of fast repetition rate (FRR) fluorescence: signatures of phytoplankton community structure versus physiological state. publication-title: Mar. Ecol. Prog. Series doi: 10.3354/meps07830 contributor: fullname: Suggett – volume: 48 start-page: 1983 year: 2001 ident: B4 article-title: Phytoplankton population dynamics at the bermuda atlantic time-series station in the Sargasso Sea. publication-title: Deep Sea Res. Part II Top. Stud. Oceanogr. doi: 10.1016/S0967-0645(00)00166-1 contributor: fullname: DuRand – volume: 8 year: 2013 ident: B12 article-title: a gene island with two possible configurations is involved in chromatic acclimation in marine Synechococcus. publication-title: PLoS One doi: 10.1371/journal.pone.0084459 contributor: fullname: Humily – volume: 142 start-page: 1255 year: 1996 ident: B2 article-title: Complementary chromatic adaptation alters photosynthetic strategies in the cyanobacterium Calothrix. publication-title: Microbiology doi: 10.1099/13500872-142-5-1255 contributor: fullname: Campbell – volume: 110 start-page: 16253 year: 2013 ident: B9 article-title: Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1306332110 contributor: fullname: Gutu – volume: 187 start-page: 1685 year: 2005 ident: B32 article-title: Two novel phycoerythrin-associated linker proteins in the marine Cyanobacterium Synechococcus sp. strain WH8102. publication-title: J. Bacteriol. doi: 10.1128/JB.187.5.1685-1694.2005 contributor: fullname: Six – volume: 51 start-page: 567 year: 2004 ident: B36 article-title: RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. publication-title: Mol. Microbiol. doi: 10.1046/j.1365-2958.2003.03853.x contributor: fullname: Terauchi – volume: 88 start-page: 231 year: 2014 ident: B11 article-title: Development of a targeted metagenomic approach to study a genomic region involved in light harvesting in marine Synechococcus. publication-title: FEMS Microbiol. Ecol. doi: 10.1111/1574-6941.12285 contributor: fullname: Humily – volume: 73 start-page: 407 ident: B24 article-title: Chromatic acclimation in cyanobacteria: a diverse and widespread process for optimizing photosynthesis. publication-title: Ann. Rev. Microbiol. doi: 10.1146/annurev-micro-020518-115738 contributor: fullname: Sanfilippo – volume: 113 start-page: 6077 year: 2016 ident: B26 article-title: Self-regulating genomic island encoding tandem regulators confers chromatic acclimation to marine Synechococcus. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1600625113 contributor: fullname: Sanfilippo – volume: 35 start-page: 17 year: 2004 ident: B30 article-title: Photophysiology of the marine cyanobacterium Synechococcus sp. WH8102, a new model organism. publication-title: Aquatic Microbial. Ecol. doi: 10.3354/ame035017 contributor: fullname: Six – volume: 138 start-page: 177 year: 2018 ident: B16 article-title: Blue light reduces photosynthetic efficiency of cyanobacteria through an imbalance between photosystems I and II. publication-title: Photosy. Res. doi: 10.1007/s11120-018-0561-5 contributor: fullname: Luimstra – volume: 172 start-page: E169 year: 2008 ident: B34 article-title: The timescale of phenotypic plasticity and its impact on competition in fluctuating environments. publication-title: Am. Nat. doi: 10.1086/591680 contributor: fullname: Stomp – volume: 19 start-page: 2348 year: 2017 ident: B17 article-title: Physiological and proteomic characterization of light adaptations in marine Synechococcus: light adaptations in marine Synechococcus. publication-title: Environ. Microbiol. doi: 10.1111/1462-2920.13744 contributor: fullname: Mackey – volume: 17 start-page: 37 year: 2019 ident: B38 article-title: Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. publication-title: Nat. Rev. Microbiol. doi: 10.1038/s41579-018-0110-4 contributor: fullname: Wiltbank – volume: 118 year: 2021 ident: B7 article-title: Molecular bases of an alternative dual-enzyme system for light color acclimation of marine Synechococcus cyanobacteria. publication-title: Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.2019715118 contributor: fullname: Grébert – volume: 188 start-page: 3345 year: 2006 ident: B5 article-title: Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. publication-title: J. Bacteriol. doi: 10.1128/JB.188.9.3345-3356.2006 contributor: fullname: Everroad – volume: 8 year: 2017 ident: B18 article-title: Adaptation to blue light in marine Synechococcus requires MpeU, an enzyme with similarity to Phycoerythrobilin lyase isomerases. publication-title: Front. Microbiol. doi: 10.3389/fmicb.2017.00243 contributor: fullname: Mahmoud – volume: 8 year: 2017 ident: B39 article-title: Synechococcus assemblages across the salinity gradient in a salt wedge estuary. publication-title: Front. Microbiol. doi: 10.3389/fmicb.2017.01254 contributor: fullname: Xia – volume: 13 start-page: 430 year: 2019 ident: B14 article-title: Parallel phylogeography of Prochlorococcus and Synechococcus. publication-title: ISME J. doi: 10.1038/s41396-018-0287-6 contributor: fullname: Kent |
SSID | ssj0001340549 |
Score | 2.228475 |
Snippet | Benefits and trade-offs of blue/green chromatic acclimation (CA4) have received limited study. We investigated the energetic costs associated with executing... |
SourceID | doaj crossref |
SourceType | Open Website Aggregation Database |
SubjectTerms | chromatic acclimation phycoerythrin plasticity Synechococcus trade-offs |
Title | Costs and Limitations of Marine Synechococcus Blue-Green Chromatic Acclimation |
URI | https://doaj.org/article/2bc7495df36c4123890d394cbe99757a |
Volume | 8 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1NS8QwEA26JxHET1y_yMGTUG2bNE2Ou7qLF9fDKngrTSYBYemK3R78906SuqwnL0JPpYTwJsy8l2ZeCLlmNa4MECaxTEPCwRaJwkqOybB2DDOiAghbF_Ny9iYfJt4mZ33Vlz8TFu2BI3B3uTYlknhwTBiOaVaqFJjiRlulyqKM1CgVG2Iq7K4wJCJcxd-YqMIUhgmFIurBPLsVqDGU_FWINvz6Q2GZ7pO9nhHSUZzJAdmyzSHZfTa2bno76SMyu1-2q5ai6qehIylus9Glo0-1b9-j86_GYiLD7Ga6lo4XnU3CiRrqzW-DKysdGbN4j42Kx-R1Onm5f0z6mxASwwq-SjJdyMzmQta14sCYzqBEbsEcK5xgQmjBHAgky5qXHITDsm-QueUaH8OFZCdk0Cwbe0qohDozzqKwK0qeulxqCVJkFkCXkEI-JDc_sFQf0fCiQqHgMawChpXHsIoYDsnYA7f-0HtVhxcYwaqPYPVXBM_-Y5BzsuPnFU5_sQsyWH129pJst9BdhZXxDYKXvE0 |
link.rule.ids | 315,782,786,866,2106,27933,27934 |
linkProvider | Directory of Open Access Journals |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Costs+and+Limitations+of+Marine+Synechococcus+Blue-Green+Chromatic+Acclimation&rft.jtitle=Frontiers+in+Marine+Science&rft.au=Raisha+Lovindeer&rft.au=Lawrence+Abbott&rft.au=Hannah+Medina&rft.au=Katherine+R.+M.+Mackey&rft.date=2021-09-03&rft.pub=Frontiers+Media+S.A&rft.eissn=2296-7745&rft.volume=8&rft_id=info:doi/10.3389%2Ffmars.2021.689998&rft.externalDBID=DOA&rft.externalDocID=oai_doaj_org_article_2bc7495df36c4123890d394cbe99757a |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=2296-7745&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=2296-7745&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=2296-7745&client=summon |