Life on the Rocks: First Insights Into the Microbiota of the Threatened Aquatic Rheophyte Hanseniella heterophylla.

Dolaya Sadubsarn,Shakhawat Hossen,Benjawan Tanunchai,Petcharat Werukamkul,Witoon Purahong,Tesfaye Wubet,Matthias Noll,Sven Dommert,Ali Nawaz,La-aw Ampornpan

doi:10.3389/fpls.2021.634960

Abstract

Little is known about microbial communities of aquatic plants despite their crucial ecosystem function in aquatic ecosystems. Here, we analyzed the microbiota of an aquatic rheophyte, Hanseniella heterophylla, growing at three areas differing in their degree of anthropogenic disturbance in Thailand employing a metabarcoding approach. Our results show that diverse taxonomic and functional groups of microbes colonize H. heterophylla. Proteobacteria, Actinobacteria, Dothideomycetes, and Sordariomycetes form the backbone of the microbiota. Surprisingly, the beneficial microbes reported from plant microbiomes in terrestrial habitats, such as N-fixing bacteria and ectomycorrhizal fungi, were also frequently detected. We showed that biofilms for attachment of H. heterophylla plants to rocks may associate with diverse cyanobacteria (distributed in eight families, including Chroococcidiopsaceae, Coleofasciculaceae, Leptolyngbyaceae, Microcystaceae, Nostocaceae, Phormidiaceae, Synechococcaceae, and Xenococcaceae) and other rock biofilm-forming bacteria (mainly Acinetobacter, Pseudomonas, and Flavobacterium). We found distinct community compositions of both bacteria and fungi at high and low anthropogenic disturbance levels regardless of the study areas. In the highly disturbed area, we found strong enrichment of Gammaproteobacteria and Tremellomycetes coupled with significant decline of total bacterial OTU richness. Bacteria involved with sulfamethoxazole (antibiotic) degradation and human pathogenic fungi (Candida, Cryptococcus, Trichosporon, and Rhodotorula) were exclusively detected as indicator microorganisms in H. heterophylla microbiota growing in a highly disturbed area, which can pose a major threat to human health. We conclude that aquatic plant microbiota are sensitive to anthropogenic disturbance. Our results also unravel the potential use of this plant as biological indicators in remediation or treatment of such disturbed ecosystems.

Highlights

Aquatic plants perform many ecosystem functions in aquatic habitats and provide services to human society (García-Llorente et al, 2011)
There were 26% of total bacterial operational taxonomic units (OTUs) detected in all study areas whereas 4, 19, and 18% were specific for Khek, Than, and San rivers, respectively
The bacterial OTU rich functions in Than and San rivers were dominated by aerobic chemoheterotrophy (Than: 94 OTUs, 34% of total functional assigned OTUs; San: 84 OTUs, 32%), cyanobacteria (Than: 35 OTUs, 13%; San: OTUs, 6%), and methane metabolism (Than: OTUs, 6%; San: 36 OTUs, 12%), while in Khek river, they belonged to aerobic chemoheterotrophy (55 OTUs, 33%), human pathogens: animal parasites or symbionts: ureolysis (13 OTUs, 9%), and N fixation (13 OTUs, 9%)

Summary

Introduction

Aquatic plants perform many ecosystem functions in aquatic habitats and provide services to human society (García-Llorente et al, 2011). One of the important functions performed by aquatic plants is the uptake of dissolved nutrients (N and P) from water (Brix, 1997). They are widely used in constructed wetlands around the world to remove excess N and P from polluted water (Vymazal, 2013). Habitat complexity provided by aquatic plants is likely to increase the richness of taxonomy and density of both fish and invertebrates (Thomaz et al, 2008). Roots of aquatic plants provide extended surface for benthic microbial communities to rest and act as a customized niche for a diverse group of microbes ensuring the continuous supply of nutrients, organic carbon, and oxygen (Stottmeister et al, 2003)

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