Transcriptional activity differentiates families of Marine Group II Euryarchaeota in the coastal ocean

Julian Damashek,Alexey Vorobev,Aimee Oyinlade Okotie-Oyekan,Scott Michael Gifford,Mary Ann Moran,James Timothy Hollibaugh

doi:10.1038/s43705-021-00002-6

Abstract

Marine Group II Euryarchaeota (Candidatus Poseidoniales), abundant but yet-uncultivated members of marine microbial communities, are thought to be (photo)heterotrophs that metabolize dissolved organic matter (DOM), such as lipids and peptides. However, little is known about their transcriptional activity. We mapped reads from a metatranscriptomic time series collected at Sapelo Island (GA, USA) to metagenome-assembled genomes to determine the diversity of transcriptionally active Ca. Poseidoniales. Summer metatranscriptomes had the highest abundance of Ca. Poseidoniales transcripts, mostly from the O1 and O3 genera within Ca. Thalassarchaeaceae (MGIIb). In contrast, transcripts from fall and winter samples were predominantly from Ca. Poseidoniaceae (MGIIa). Genes encoding proteorhodopsin, membrane-bound pyrophosphatase, peptidase/proteases, and part of the ß-oxidation pathway were highly transcribed across abundant genera. Highly transcribed genes specific to Ca. Thalassarchaeaceae included xanthine/uracil permease and receptors for amino acid transporters. Enrichment of Ca. Thalassarchaeaceae transcript reads related to protein/peptide, nucleic acid, and amino acid transport and metabolism, as well as transcript depletion during dark incubations, provided further evidence of heterotrophic metabolism. Quantitative PCR analysis of South Atlantic Bight samples indicated consistently abundant Ca. Poseidoniales in nearshore and inshore waters. Together, our data suggest that Ca. Thalassarchaeaceae are important photoheterotrophs potentially linking DOM and nitrogen cycling in coastal waters.

Highlights

Metagenomic studies provided the first evidence that Marine Group II (MGII) may be aerobic heterotrophs,[5,6,7] a hypothesis supported by incubation experiments[8,9,10] and by the gene content of diverse metagenomeassembled genomes (MAGs).[11,12,13,14,15]
Two recent studies deepened our understanding of the phylogenomics and metabolic potential of MGII by analyzing hundreds of MAGs, highlighting clade-specific differences in genomic potential for transport and degradation of organic molecules, light-harvesting proteorhodopsins, and motility.[16,17]
Proton gradients and electron transport Our analysis revealed that Ca Poseidoniales genes involved in establishing transmembrane proton gradients were highly transcribed in our samples

Summary

Introduction

Since the initial discovery of Marine Group II (MGII) Euryarchaeota,[1,2] definitive determination of their physiology and ecological roles has remained challenging due to the lack of a cultivated isolate.as data describing MGII distributions throughout the ocean have increased, several patterns have emerged: MGII is often highly abundant in the euphotic zone and in coastal waters, can reach high abundance following phytoplankton blooms, and largely comprised two subclades, MGIIa and MGIIb.[3,4] Early metagenomic studies provided the first evidence that MGII may be aerobic (photo) heterotrophs,[5,6,7] a hypothesis supported by incubation experiments[8,9,10] and by the gene content of diverse metagenomeassembled genomes (MAGs).[11,12,13,14,15] Two recent studies deepened our understanding of the phylogenomics and metabolic potential of MGII by analyzing hundreds of MAGs, highlighting clade-specific differences in genomic potential for transport and degradation of organic molecules, light-harvesting proteorhodopsins, and motility.[16,17] Here, we refer to MGII as the putative order “Candidatus Poseidoniales,” MGIIa and MGIIb as the putative families “Ca. Poseidoniaceae” and “Ca. Thalassarchaeaceae,” respectively, and putative genera as specified by Rinke et al.[16]. We occasionally use “MGIIa” and “MGIIb” for consistency with previous literature

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Discussion

Conclusion