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Niche Differentiation Among Annually Recurrent Coastal Marine Group II Euryarchaeota

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Niche Differentiation Among Annually Recurrent Coastal Marine Group II Euryarchaeota The ISME Journal (2019) 13:3024–3036 https://doi.org/10.1038/s41396-019-0491-z ARTICLE Niche differentiation among annually recurrent coastal Marine Group II Euryarchaeota 1 1 1 1 1 Luis H. Orellana ● T. Ben Francis ● Karen Krüger ● Hanno Teeling ● Marie-Caroline Müller ● 1 2 1 Bernhard M. Fuchs ● Konstantinos T. Konstantinidis ● Rudolf I. Amann Received: 25 March 2019 / Revised: 26 July 2019 / Accepted: 29 July 2019 / Published online: 26 August 2019 © The Author(s) 2019. This article is published with open access Abstract Since the discovery of archaeoplankton in 1992, the euryarchaeotal Marine Group II (MGII) remains uncultured and less understood than other planktonic archaea. We characterized the seasonal dynamics of MGII populations in the southern North Sea on a genomic and microscopic level over the course of four years. We recovered 34 metagenome-assembled genomes (MAGs) of MGIIa and MGIIb that corroborated proteorhodopsin-based photoheterotrophic lifestyles. However, MGIIa and MGIIb MAG genome sizes differed considerably (~1.9 vs. ~1.4 Mbp), as did their transporter, peptidase, flagella and sulfate assimilation gene repertoires. MGIIb populations were characteristic of winter samples, whereas MGIIa 1234567890();,: 1234567890();,: accounted for up to 23% of the community at the beginning of summer. Both clades consisted of annually recurring, sequence-discrete populations with low intra-population sequence diversity. Oligotyping of filtered cell-size fractions and microscopy consistently suggested that MGII cells were predominantly free-living. Cells were coccoid and ~0.7 µm in diameter, likely resulting in grazing avoidance. Based on multiple lines of evidence, we propose distinct niche adaptations of MGIIa and MGIIb Euryarchaeota populations that are characteristic of summer and winter conditions in the coastal North Sea. Introduction mostly associated with deep sea environments. So far, only members of the MGI group have been isolated [9]. Thus, Since the discovery of marine planktonic archaea using the characterization of other marine archaea has been lim- culture-independent approaches [1, 2], four major archaeal ited to culture-independent approaches. MGI have been lineages have been characterized in marine ecosystems. The mostly associated with ammonia oxidation [9], whereas less thaumarchaeotal Marine Group I (MGI) and the eur- is known about MGII. Nonetheless, sequences recovered yarchaeotal Marine Group II (MGII) have been found in from metagenomes belonging to the MGIIa subgroup have deep and surface ocean waters, respectively [3–5]. In suggested a potential role in protein and fatty acid degra- addition, archaea belonging to the euryarchaeotal Marine dation [10–12]. It has been proposed that MGII could thrive Group III (MGIII) [6, 7] and IV (MGIV) [8] have been under oligotrophic conditions, where particle-associated MGII can outnumber free-living cells of the same group [13]. In addition, a partially recovered genome of the MGIIb group (originally proposed as class ‘Thalassoarch- Supplementary information The online version of this article (https:// aea’), obtained from the Mediterranean deep chlorophyll doi.org/10.1038/s41396-019-0491-z) contains supplementary material, maximum, showed similar heterotrophic features as those which is available to authorized users. found in MGIIa genomes, but have a lower GC percentage * Rudolf I. Amann and a smaller genome size [14]. Hence the high diversity [email protected] recently reported [11, 12] within MGII populations under- scores the knowledge gaps for these marine archaeal clades. 1 Department of Molecular Ecology, Max Planck Institute for Marine Microbiology, Bremen D-28359, Germany Our understanding of the dynamics of MGII populations 2 has until recently [11, 12] been restricted to the use of School of Civil and Environmental Engineering, Georgia Institute – of Technology, Ford Environmental Science and Technology molecular markers such as 16S rRNA gene sequences [15 Building, 311 Ferst Drive, Atlanta, GA 30332, USA 17]. Studies in the Mediterranean have suggested niche Niche differentiation among annually recurrent coastal Marine Group II Euryarchaeota 3025 separation between MGI and MGII, but also within MGII passed through 10 and 3 µm pore-size filters before cells populations. For instance, while MGIIb (and MGI) domi- were collected on 0.2 µm pore-size polycarbonate filters. nated at the time of winter sampling, MGIIa were abundant This approach removed phytoplankton and most of the during summer. These seasonal differences were proposed particle-associated microorganisms. Seawater for cell to result from strong changes in biotic (e.g., nutrient and counting was also collected from the surface, but it was not phytoplankton stocks) and abiotic factors (e.g., temperature fractionated [23, 26]. The sequencing of 44 surface water and water column stratification) over the winter-summer metagenomes from ‘Kabeltonne’ was performed at the DOE transition [15]. Previous reports have indicated short Joint Genome Institute (DOE-JGI) as described previously blooms of MGII populations during summer [3, 15, 18] [25, 26]. Metagenomes from 2009 [23] were sequenced on following phytoplankton bloom events and also coinciding the GS FLX Ti platform (454 Life Sciences, Branfort, CT, with decreased levels of chlorophyll a [17, 19]. Phyto- USA), all others on the Illumina HiSeq platform (Illumina, plankton blooms in coastal marine environments often San Diego, CA, USA) with paired-end sequencing [25]. cause successions of bacterioplankton communities parti- Trimming and processing of raw reads was performed as cipating in the remineralization of the released organic previously published [26]. matter [20], which are dominated by members of the classes Flavobacteriia, Alphaproteobacteria and Gammaproteo- Catalyzed reporter deposition fluorescence in situ bacteria [21–23]. Still, the diversity of MGII populations hybridization occurring before and after these blooms have received much less attention due to their usually lower abundance com- For the enumeration of Euryarchaeota, 100 ml of water pared to heterotrophic bacterioplankton [17, 24]. A recent were fixed with 1% formaldehyde at room temperature for large phylogenomic comparison of MGII flagellum-based 1h,filtered onto 47 mm diameter polycarbonate filters (pore adhesion, transport and degradative potential suggests that size 0.2 µm) with a vacuum of at most 100 mbar. Catalyzed multiple MGII clades diversified from a surface water- Reporter Deposition Fluorescence in situ hybridization dwelling photoheterotrophic ancestor [11]. However, little (CARD-FISH) was performed as outlined before [27]. A is known about how the genomic potential of distinct MGII detailed protocol is available in the supplementary text. clades correlates with observed temporal abundance pat- terns. In addition, not much is known about the level of MAG recovery genetic heterogeneity within recurrent MGII populations, which is important for delimiting MGII ecophysiological Archaeal MAGs were obtained from previously assembled niches including ecotypes and their impact on coastal 2010–2012 Helgoland metagenomes [26]. Briefly, de novo environments. assembly of short-read metagenomes was performed using We combined fluorescence in situ hybridization (FISH) SPADES 3.10 [28] and assembled contigs longer than and metagenome sequencing approaches to explore the 2.5 kbp were binned using CONCOCT [29] as part of the temporal patterns and metabolic potentials of discrete eur- standard Anvi’o v3 metagenomic workflow [30]. Differ- yarchaeotal populations in the southern North Sea (German ential coverage information was generated by mapping Bight) in the years 2009 to 2012. The recovery of 34 high- reads from four additional randomly selected dates from the quality metagenome-assembled genomes (MAGs) related to same year. Reads were mapped using BBMap v35.14 MGII allowed us to compare the genomes and ecology of (http://bbtools.jgi.doe.gov; ‘fast’ mode, minid = 0.99, and MGIIa and MGIIb. Our results reveal low intra-population idfilter = 0.97). Manual inspection for congruent genetic diversity of annually recurrent MGII populations and pro- composition and coverage of recovered MAGs was per- vides novel information on the potential niche differentia- formed in Anvi’o[30]. Selected MAGs (%[completion] tion of summer and winter clades of photoheterotrophic −4 × % [contamination] ≥ 50 (determined by checkM [31])) Marine Group II Euryarchaeota. were de-replicated using dRep v2.2.3 [32], which combines MASH and average nucleotide identity (ANI > 95%) mea- sures in order to select the best representative from each Materials and methods group of highly similar MAGs (Table S1). Genes were predicted using Prodigal v2.6.3 [33] (metagenome option). Sampling and sequencing Reported taxonomic classification, completion and con- tamination for archaeal MAGs was determined using the Surface seawater samples were collected from the ‘Kabel- Microbial Genome Atlas webserver (MiGA) [34]. MAGs tonne’ ecological research site off the North Sea island of were uploaded to MiGA using the “popgenome” dataset Helgoland (54◦ 11.3′ N, 7◦ 54.0′ E) as described previously option. MiGA determines completeness and contamination [23, 25, 26]. Briefly, samples for DNA sequencing were using previously reported single-copy marker genes [35]. 3026 L. H. Orellana et al. Taxonomic classifications are based on genome-aggregate discontinuity for mapped reads was selected upon visual average amino acid and average
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