Seagrass Colonization Alters Diversity, Abundance, Taxonomic, and Functional Community Structure of Benthic Microbial Eukaryotes

Ying Pan; Guihao Li; Lei Su; Pengfei Zheng; Yaping Wang; Zhuo Shen; Zigui Chen; Qiuying Han; Jun Gong

doi:10.3389/fmicb.2022.901741

Seagrass Colonization Alters Diversity, Abundance, Taxonomic, and Functional Community Structure of Benthic Microbial Eukaryotes

Front Microbiol. 2022 Jun 13:13:901741. doi: 10.3389/fmicb.2022.901741. eCollection 2022.

Authors

Ying Pan¹, Guihao Li², Lei Su³, Pengfei Zheng³, Yaping Wang², Zhuo Shen², Zigui Chen⁴, Qiuying Han⁵, Jun Gong^{2

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Affiliations

¹ School of Ecology, Sun Yat-sen University, Shenzhen, China.
² Laboratory of Microbial Ecology and Matter Cycle, School of Marine Sciences, Sun Yat-sen University, Zhuhai, China.
³ Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, China.
⁴ Department of Microbiology, The Chinese University of Hong Kong, Hong Kong, China.
⁵ College of Ecology and Environment, Hainan Tropical Ocean University, Sanya, China.
⁶ Southern Marine Science and Engineering Guangdong Laboratory, Zhuhai, China.
⁷ Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, Guangzhou, China.

Abstract

Seagrass form high productive ecosystems in coastal environments. However, the effects of these coastal plants on the structure and function of the belowground eukaryotic microbiome remain elusive. In this study, we characterized the community of microbial eukaryotes (microeukaryotes) in both vegetated and unvegetated sediments using 18S rRNA gene amplicon sequencing and quantitative PCR. Analysis of sequencing data showed that the eelgrass (Zostera marina) colonization decreased the alpha diversity indices of benthic microeukaryotes. Apicomplexa represented an average of 83% of reads across all samples, with a higher proportion at the vegetated sites. The taxonomic community structure was significantly different between these two types of sediments, for which the concentration of ${NH}_{4}^{+}$ in sediment porewater and salinity could account. Phylogenetic analyses of long 18S rRNA genes (around 1,030 bp) indicated these apicomplexan parasites are closely related to gregarine Lecudina polymorpha. Determination of 18S rRNA gene abundances provided evidence that the eelgrass markedly promoted the biomass of the gregarine and all microeukaryotes in the seagrass-colonized sediments and confirmed that the gregarine was hosted by a polychaete species. Significantly higher gene abundances of heterotrophs and mixotrophs were found at the vegetated sites, which could be explained by the finer sediments and short supply of dissolved inorganic nitrogen, respectively. The pigmented protists were more abundant in 18S rRNA gene copies at the lower and higher pH levels than at the intermediate. Nevertheless, the fractions of heterotrophs and phototrophs in the community were significantly related to porewater N:P ratio. These results indicate that seagrass colonization significantly induces an increase in overall biomass and a decrease in diversity of benthic microeukaryotes, making them more heterotrophic. This study also highlights that the hotspot of eukaryotic parasites could be linked with the high productivity of a natural ecosystem.

Keywords: belowground diversity; community structure; functional composition; high throughput sequencing; parasite; protist.