Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding

ABSTRACTMicroeukaryotic plankton (0.2–200 µm), which are morphologically and genetically highly diverse, play a crucial role in ocean productivity and carbon consumption. The Pacific Ocean (PO), one of the world’s largest oligotrophic regions, remains largely unexplored in terms of the biogeography...

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Main Authors: Yingjun Fu, Zhishuai Qu, Ying Wang, Ping Sun, Nianzhi Jiao, Dapeng Xu
Format: Article
Language:English
Published: American Society for Microbiology 2024-04-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.02424-23
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author Yingjun Fu
Zhishuai Qu
Ying Wang
Ping Sun
Nianzhi Jiao
Dapeng Xu
author_facet Yingjun Fu
Zhishuai Qu
Ying Wang
Ping Sun
Nianzhi Jiao
Dapeng Xu
author_sort Yingjun Fu
collection DOAJ
description ABSTRACTMicroeukaryotic plankton (0.2–200 µm), which are morphologically and genetically highly diverse, play a crucial role in ocean productivity and carbon consumption. The Pacific Ocean (PO), one of the world’s largest oligotrophic regions, remains largely unexplored in terms of the biogeography and biodiversity of microeukaryotes based on large-scale sampling. We investigated the horizontal distribution of microeukaryotes along a 16,000 km transect from the west to the east of the PO. The alpha diversity indices showed a distinct decreasing trend from west to east, which was highly correlated with water temperature. The microeukaryotic community, which was clustered into the western, central, and eastern PO groups, displayed a significant distance-decay relationship. Syndiniales, a lineage of parasitic dinoflagellates, was ubiquitously distributed along the transect and dominated the community in terms of both sequence and zero-radius operational taxonomic unit (ZOTU) proportions. The prevailing dominance of Syndiniales-affiliated ZOTUs and their close associations with dinoflagellates, diatoms, and radiolarians, as revealed by SparCC correlation analysis, suggested that parasitism may be an important trophic strategy in the surface waters of the PO. Geographical distance and temperature were the most important environmental factors that significantly correlated with community structure. Overall, our study sheds more light on the distribution pattern of both alpha and beta diversities of microeukaryotic communities and highlighted the importance of parasitisms by Syndiniales across the tropical PO.IMPORTANCEUnderstanding the biogeographical and biodiversity patterns of microeukaryotic communities is essential to comprehending their roles in biogeochemical cycling. In this study, planktonic microeukaryotes were collected along a west-to-east Pacific Ocean transect (ca. 16,000 km). Our study revealed that the alpha diversity indices were highly correlated with water temperature, and the microeukaryotic communities displayed a distinct geographical distance-driven pattern. The predominance of the parasitic dinoflagellate lineage Syndiniales and their close relationship with other microeukaryotic groups suggest that parasitism may be a crucial survival strategy for microeukaryotes in the surface waters of the Pacific Ocean. Our findings expand our understanding of the biodiversity and biogeographical pattern of microeukaryotes and highlight the significance of parasitic Syndiniales in the surface ocean.
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spelling doaj.art-71cea3034bca401a92fd679dbb6d418d2024-04-02T14:16:19ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972024-04-0112410.1128/spectrum.02424-23Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcodingYingjun Fu0Zhishuai Qu1Ying Wang2Ping Sun3Nianzhi Jiao4Dapeng Xu5State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, ChinaInstitute of Marine Science and Technology, Shandong University, Qingdao 266237, ChinaKey Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, Fujian Provincial Key Laboratory of Coastal Ecology and Environmental Studies, College of the Environment and Ecology, Xiamen University, Xiamen, ChinaKey Laboratory of Ministry of Education for Coastal and Wetland Ecosystems, Fujian Provincial Key Laboratory of Coastal Ecology and Environmental Studies, College of the Environment and Ecology, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, ChinaState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University, Xiamen, ChinaABSTRACTMicroeukaryotic plankton (0.2–200 µm), which are morphologically and genetically highly diverse, play a crucial role in ocean productivity and carbon consumption. The Pacific Ocean (PO), one of the world’s largest oligotrophic regions, remains largely unexplored in terms of the biogeography and biodiversity of microeukaryotes based on large-scale sampling. We investigated the horizontal distribution of microeukaryotes along a 16,000 km transect from the west to the east of the PO. The alpha diversity indices showed a distinct decreasing trend from west to east, which was highly correlated with water temperature. The microeukaryotic community, which was clustered into the western, central, and eastern PO groups, displayed a significant distance-decay relationship. Syndiniales, a lineage of parasitic dinoflagellates, was ubiquitously distributed along the transect and dominated the community in terms of both sequence and zero-radius operational taxonomic unit (ZOTU) proportions. The prevailing dominance of Syndiniales-affiliated ZOTUs and their close associations with dinoflagellates, diatoms, and radiolarians, as revealed by SparCC correlation analysis, suggested that parasitism may be an important trophic strategy in the surface waters of the PO. Geographical distance and temperature were the most important environmental factors that significantly correlated with community structure. Overall, our study sheds more light on the distribution pattern of both alpha and beta diversities of microeukaryotic communities and highlighted the importance of parasitisms by Syndiniales across the tropical PO.IMPORTANCEUnderstanding the biogeographical and biodiversity patterns of microeukaryotic communities is essential to comprehending their roles in biogeochemical cycling. In this study, planktonic microeukaryotes were collected along a west-to-east Pacific Ocean transect (ca. 16,000 km). Our study revealed that the alpha diversity indices were highly correlated with water temperature, and the microeukaryotic communities displayed a distinct geographical distance-driven pattern. The predominance of the parasitic dinoflagellate lineage Syndiniales and their close relationship with other microeukaryotic groups suggest that parasitism may be a crucial survival strategy for microeukaryotes in the surface waters of the Pacific Ocean. Our findings expand our understanding of the biodiversity and biogeographical pattern of microeukaryotes and highlight the significance of parasitic Syndiniales in the surface ocean.https://journals.asm.org/doi/10.1128/spectrum.02424-23microbial eukaryotesprotistsSyndinialesSSU rRNA genehigh throughput sequencing
spellingShingle Yingjun Fu
Zhishuai Qu
Ying Wang
Ping Sun
Nianzhi Jiao
Dapeng Xu
Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
Microbiology Spectrum
microbial eukaryotes
protists
Syndiniales
SSU rRNA gene
high throughput sequencing
title Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
title_full Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
title_fullStr Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
title_full_unstemmed Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
title_short Biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern Pacific Ocean transect revealed by metabarcoding
title_sort biogeographical and biodiversity patterns of planktonic microeukaryotes along the tropical western to eastern pacific ocean transect revealed by metabarcoding
topic microbial eukaryotes
protists
Syndiniales
SSU rRNA gene
high throughput sequencing
url https://journals.asm.org/doi/10.1128/spectrum.02424-23
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