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Seasonality of Archaeal Proteorhodopsin and Associated Marine Group Iib Ecotypes (Ca The ISME Journal (2021) 15:1302–1316 https://doi.org/10.1038/s41396-020-00851-4 ARTICLE Seasonality of archaeal proteorhodopsin and associated Marine Group IIb ecotypes (Ca. Poseidoniales) in the North Western Mediterranean Sea 1,5 1 2 3 4 Olivier Pereira ● Corentin Hochart ● Dominique Boeuf ● Jean Christophe Auguet ● Didier Debroas ● Pierre E. Galand 1 Received: 23 July 2020 / Revised: 9 November 2020 / Accepted: 18 November 2020 / Published online: 7 December 2020 © The Author(s), under exclusive licence to International Society for Microbial Ecology 2020 Abstract The Archaea Marine Group II (MGII) is widespread in the world’s ocean where it plays an important role in the carbon cycle. Despite recent discoveries on the group’s metabolisms, the ecology of this newly proposed order (Candidatus Poseidoniales) remains poorly understood. Here we used a combination of time-series metagenome-assembled genomes (MAGs) and high-frequency 16S rRNA data from the NW Mediterranean Sea to test if the taxonomic diversity within the MGIIb family (Candidatus Thalassarchaeaceae) reflects the presence of different ecotypes. The MAGs’ seasonality revealed 1234567890();,: 1234567890();,: a MGIIb family composed of different subclades that have distinct lifestyles and physiologies. The vitamin metabolisms were notably different between ecotypes with, in some, a possible link to sunlight’s energy. Diverse archaeal proteorhodopsin variants, with unusual signature in key amino acid residues, had distinct seasonal patterns corresponding to changing day length. In addition, we show that in summer, archaea, as opposed to bacteria, disappeared completely from surface waters. Our results shed light on the diversity and the distribution of the euryarchaeotal proteorhodopsin, and highlight that MGIIb is a diverse ecological group. The work shows that time-series based studies of the taxonomy, seasonality, and metabolisms of marine prokaryotes is critical to uncover their diverse role in the ocean. Introduction These authors contributed equally: Olivier Pereira, Corentin Hochart, Dominique Boeuf Planktonic archaea were first detected in the sea almost 30 Supplementary information The online version of this article (https:// years ago [1, 2]. Since then, the extent of the diversity, doi.org/10.1038/s41396-020-00851-4) contains supplementary material, which is available to authorized users. distribution, and potential function of the third domain of life in the ocean has been extensively studied, but many * Pierre E. Galand unknowns remain. Among marine Archaea, the Marine [email protected] Group II (MGII) is usually more prevalent in surface 1 Sorbonne Universités, CNRS, Laboratoire d’Ecogéochimie des waters, but not always, and has a global distribution from Environnements Benthiques (LECOB), Observatoire the poles to tropical seas [3]. Its widespread occurrence Océanologique, Banyuls sur Mer, France suggested that it had an important role in the ocean, but 2 Daniel K. Inouye Center for Microbial Oceanography, Research because of the lack of any cultivated representatives, its and Education, School of Ocean and Earth Science and physiology was largely unknown. The development of ‘ ā Technology, University of Hawai iatMnoa, Honolulu, HI, metagenomic approaches has, however, allowed a glimpse United States, Honolulu, HI 96822, USA into the metabolic potential and lifestyle of the MGII [4– 3 MARBEC, Université de Montpellier, CNRS, Ifremer, IRD, 10]. Some MGII harbor a proteorhodopsin (PR) gene and Montpellier, France, Montpellier, France could thus be able to use sunlight as energy source 4 Université Clermont Auvergne, CNRS, Laboratoire [11, 12]. They can potentially degrade large molecules Microorganismes: Genome et Environnement, 63000 Clermont- Ferrand, France such as lipids, proteins, and polysaccharides [8, 9, 12], and some have genes for motility [6, 7, 12]. The rare 5 Present address: Shenzhen Key Laboratory of Marine Archaea Geo-Omics, Southern University of Science and Technology, experimental tests of the metabolisms of MGII showed the Shenzhen, China uptake of phytoplankton-derived proteins using stable- Seasonality of archaeal proteorhodopsin and associated Marine Group IIb ecotypes (Ca. Poseidoniales). 1303 isotope probing [13],andstimulatedgrowthinthepre- Materials and methods sence of whole cells of the picoeukaryote Micromonas [9]. The potential metabolisms detected in MGII suggest Sampling and metagenome sequencing that the group has an important role for the carbon cycle of the ocean [14]. For metagenome data, surface seawater (3 m) was collected Among the genes present in MGII, the archaeal PR has monthly from January 2012 to February 2015 (40 samples) some interesting features. Analyses of key amino acid at the SOLA station (42°31′N, 03°11′E) in the Bay of residues show that both green- and blue-light tuned PR Banyuls sur Mer (France) in the northwestern Mediterra- types are present within the group [6, 7], with distinct nean as described previously [23]. Briefly, a volume of 5 L geographic and vertical distributions [10]. The archaeal PR was prefiltered through 3-μm pore-size polycarbonate fil- phylogeny is very different from the inferred organismal ters (Millipore, Billerica, MA, USA), and the microbial phylogeny [6], which indicates extensive and ongoing biomass was collected on 0.22-μm pore-size GV Sterivex horizontal gene transfers [11, 15]. Although the rhodopsins cartridges (Millipore). The physicochemical parameters found in this pelagic archaeal group are predicted to act as a were provided by the Service d’ObservationenMilieu counter-gradient protonic pumps, like canonical PRs, the Littoral (SOMLIT). Metagenomes were sequenced on a fact that some genes have a very unusual amino acid HiSeq 2500 “High-Output” paired-end run (2 × 100 bp) sequences [4], and that some MGII can grow in the dark [9], (Illumina). Sequencing produced a total of 2,984,444,036 begs additional examination of the genomic diversity and reads that were archived in the EBI repository under the ecology of the archaeal PRs. accession number PRJEB26919. MGII was recently proposed as an order level lineage, Candidatus Poseidoniales, separated in two families: MGIIa Gene catalog (Candidatus Poseidonaceae) and MGIIb (Candidatus Tha- lassarchaeaceae) [6]. The two families have different spatial A gene catalog was built as described earlier [23]. Briefly, and temporal distributions, with MGIIb generally found in for each metagenome, high-quality reads were individually deeper waters [4, 10, 16–18], and in surface waters during assembled with IDBA-UD [24], and gene prediction was winter in temperate seas, while MGIIa is predominant in done on contigs ≥1 kb with MetaGeneAnnotator [25], which summer [19–21]. These different distributions suggest that generated a total of 6.4 million gene-coding sequences. A the two groups have different ecologic niches correspond- catalog of genes was then built by clustering the predicted ing to distinct lifestyles [3]. The specific metabolic traits gene-coding sequences at 95% identity using CD-HIT (v. distinguishing MGIIa and MGIIb were recently described 4.6, [26]. The resulting catalog contained 1,568,213 non- more in details [4, 6, 7, 21, 22]. For example, members of redundant predicted genes for the SOLA site. An abundance the MGIIa have a larger genome size [7, 21], they are all matrix of gene-coding sequences was then built by mapping motile and have a catalase gene possibly protecting the cell the metagenomic reads against the predicted SOLA gene from oxidative damage [22], while MGIIb have the poten- catalog using the SOAPaligner [27]. The abundance matrix tial for assimilatory sulfate reduction [4, 21]. The fact that was normalized to the gene length and per million of reads. MGIIa and MGIIb represent different taxonomic and eco- The 16S rRNA gene contigs were annotated against the logical entities is now clear, but the question remains as SILVA database (v.128). whether the large phylogenetic diversity seen within each family, and especially within MGIIb, reflects the presence Metagenomic co-assemblies and binning of additional ecotypes. The main goal of this study was to test for the presence The 40 metagenomes were first compared to each other with of different ecotypes within the diverse MGIIb family. In the Commet software [28] to assess their pairwise similar- addition, we wanted to study if different archaeal PR ity. The method allows an all-against-all comparison of the groups reflect different ecological strategies within MGII non-assembled reads based on shared k-mers. The cluster- archaea. To do so, we used a metagenomic time series ing of metagenomes according to their k-mer similarity gathered over 3 years at the SOLA station in the Bay of separated samples in four groups that corresponded to the Banyuls sur Mer in the North Western Mediterranean Sea four seasons: winter, spring, summer, and autumn (Sup- [23]. We reconstructed metagenome-assembled genomes plementary Fig. 1). We then co-assembled all reads that (MAGs) and monitored their seasonal dynamics monthly. belonged to a same seasonal group using MEGAHIT We also used a high-frequency (twice a week) 16S rRNA (v.1.1.1) with the ‘meta-sensitive’ preset parameter [29]. amplicon sampling to track the fine succession of Contig abundance profiles were produced by mapping back ecotypes. short reads to the co-assemblies using the mem algorithm 1304 O. Pereira et al. from BWA (v.0.7.12) [30]. We then clustered contigs >2.5 corresponding to HMM hits were generated using prodigal kbp with the automatic binning algorithm CONCOCT (v.2.6.3, [36]). The corresponding protein sequences were (v.1.0.0) with a maximal number of clusters set to 100 to dereplicated then clustered into PR sequence clusters (PR minimize the ‘fragmentation error’ [31]. Finally, we clusters) at a conservative value of 82% amino acid manually binned each CONCOCT cluster using the anvi’o sequence similarity as used earlier [43]. The clustering was interactive interface to produce MAGs [32]. done using CD-HIT (v.4.7, [26]) with parameters set as “-c 1-n5-p1-T6-g1-d0” and “-c 0.82 -n 5 -p 1 -T 6 -g 1 -d Identification and selection of MAGs 0”, respectively.
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