Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution

Microbial proton-pump rhodopsin (PPR)-based phototrophy, a light-harvesting mechanism different from chlorophyll-based photosystems, may contribute significantly to solar energy entry into the marine ecosystem. PPR transforms solar energy into cellular energy that is used for various metabolic proce...

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Main Authors: Huan Zhang, Kelly J. Nulick, Zair Burris, Melissa Pierce, Minglei Ma, Senjie Lin
Format: Article
Language:English
Published: MDPI AG 2024-03-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/12/3/628
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author Huan Zhang
Kelly J. Nulick
Zair Burris
Melissa Pierce
Minglei Ma
Senjie Lin
author_facet Huan Zhang
Kelly J. Nulick
Zair Burris
Melissa Pierce
Minglei Ma
Senjie Lin
author_sort Huan Zhang
collection DOAJ
description Microbial proton-pump rhodopsin (PPR)-based phototrophy, a light-harvesting mechanism different from chlorophyll-based photosystems, may contribute significantly to solar energy entry into the marine ecosystem. PPR transforms solar energy into cellular energy that is used for various metabolic processes in the cells or flagellar movement. Although rhodopsins or their encoding genes have been documented in a wide phylogenetic range of cultured dinoflagellates, information is limited about how widespread and how spatiotemporally dynamical dinoflagellate PPR (DiPPR) are in natural marine ecosystems. In this study, we investigated DiPPR in Long Island Sound (LIS), a temperate estuary of the Atlantic Ocean between Connecticut and Long Island, New York, USA. We isolated six novel full-length dinoflagellate proton-pump rhodopsin cDNAs, expanding the DiPPR database that is crucial to PPR research. Based on these new sequences and existing sequences of DiPPR, we designed primers and conducted quantitative PCR and sequencing to determine the abundance and diversity of DiPPR genes spatially and temporally throughout a year in the water samples collected from LIS. DiPPR genes were found year-round and throughout LIS but with higher abundances in the eutrophic Western Sound and in April and July. The gene diversity data suggest that there are at least five distinct rhodopsin-harboring groups of dinoflagellates throughout the year. The abundance of DiPPR genes, measured as copy number per mL of seawater, appeared not to be influenced by water temperature or nitrogen nutrient concentration but exhibited weak negative correlations with orthophosphate concentration and salinity and a positive correlation with the abundance of DiPPR-harboring dinoflagellates. This first quantitative profiling of PPR in natural plankton reveals the prevalence and dynamics of this plastid-independent photoenergy harvesting mechanism in a temperate estuary and provides efficient DiPPR primers potentially useful for future research. Furthermore, this study shed light on the potential role of DiPPR in phosphor nutrition and dinoflagellate population, which warrants further studies.
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spelling doaj.art-4607a3c096714dd186288f02378ba4892024-03-27T13:56:02ZengMDPI AGMicroorganisms2076-26072024-03-0112362810.3390/microorganisms12030628Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal DistributionHuan Zhang0Kelly J. Nulick1Zair Burris2Melissa Pierce3Minglei Ma4Senjie Lin5Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USADepartment of Marine Sciences, University of Connecticut, Groton, CT 06340, USADepartment of Marine Sciences, University of Connecticut, Groton, CT 06340, USADepartment of Marine Sciences, University of Connecticut, Groton, CT 06340, USAState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Xiamen University, Xiamen 361102, ChinaDepartment of Marine Sciences, University of Connecticut, Groton, CT 06340, USAMicrobial proton-pump rhodopsin (PPR)-based phototrophy, a light-harvesting mechanism different from chlorophyll-based photosystems, may contribute significantly to solar energy entry into the marine ecosystem. PPR transforms solar energy into cellular energy that is used for various metabolic processes in the cells or flagellar movement. Although rhodopsins or their encoding genes have been documented in a wide phylogenetic range of cultured dinoflagellates, information is limited about how widespread and how spatiotemporally dynamical dinoflagellate PPR (DiPPR) are in natural marine ecosystems. In this study, we investigated DiPPR in Long Island Sound (LIS), a temperate estuary of the Atlantic Ocean between Connecticut and Long Island, New York, USA. We isolated six novel full-length dinoflagellate proton-pump rhodopsin cDNAs, expanding the DiPPR database that is crucial to PPR research. Based on these new sequences and existing sequences of DiPPR, we designed primers and conducted quantitative PCR and sequencing to determine the abundance and diversity of DiPPR genes spatially and temporally throughout a year in the water samples collected from LIS. DiPPR genes were found year-round and throughout LIS but with higher abundances in the eutrophic Western Sound and in April and July. The gene diversity data suggest that there are at least five distinct rhodopsin-harboring groups of dinoflagellates throughout the year. The abundance of DiPPR genes, measured as copy number per mL of seawater, appeared not to be influenced by water temperature or nitrogen nutrient concentration but exhibited weak negative correlations with orthophosphate concentration and salinity and a positive correlation with the abundance of DiPPR-harboring dinoflagellates. This first quantitative profiling of PPR in natural plankton reveals the prevalence and dynamics of this plastid-independent photoenergy harvesting mechanism in a temperate estuary and provides efficient DiPPR primers potentially useful for future research. Furthermore, this study shed light on the potential role of DiPPR in phosphor nutrition and dinoflagellate population, which warrants further studies.https://www.mdpi.com/2076-2607/12/3/628dinoflagellateproton pump rhodopsinspatial/seasonal variationqPCRLIStemperate estuary
spellingShingle Huan Zhang
Kelly J. Nulick
Zair Burris
Melissa Pierce
Minglei Ma
Senjie Lin
Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
Microorganisms
dinoflagellate
proton pump rhodopsin
spatial/seasonal variation
qPCR
LIS
temperate estuary
title Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
title_full Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
title_fullStr Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
title_full_unstemmed Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
title_short Dinoflagellate Proton-Pump Rhodopsin Genes in Long Island Sound: Diversity and Spatiotemporal Distribution
title_sort dinoflagellate proton pump rhodopsin genes in long island sound diversity and spatiotemporal distribution
topic dinoflagellate
proton pump rhodopsin
spatial/seasonal variation
qPCR
LIS
temperate estuary
url https://www.mdpi.com/2076-2607/12/3/628
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