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Ecologically Coherent Population Structure of Uncultivated Bacterioplankton

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Ecologically Coherent Population Structure of Uncultivated Bacterioplankton The ISME Journal (2021) 15:3034–3049 https://doi.org/10.1038/s41396-021-00985-z ARTICLE Ecologically coherent population structure of uncultivated bacterioplankton 1,2 1 1 1 Conny Sjöqvist ● Luis Fernando Delgado ● Johannes Alneberg ● Anders F. Andersson Received: 4 December 2020 / Revised: 31 March 2021 / Accepted: 9 April 2021 / Published online: 5 May 2021 © The Author(s) 2021. This article is published with open access Abstract Bacterioplankton are main drivers of biogeochemical cycles and important components of aquatic food webs. While sequencing-based studies have revealed how bacterioplankton communities are structured in time and space, relatively little is known about intraspecies diversity patterns and their ecological relevance. Here, we use the newly developed software POGENOM (POpulation GENomics from Metagenomes) to investigate genomic diversity and differentiation in metagenome-assembled genomes from the Baltic Sea, and investigate their genomic variation using metagenome data spanning a 1700 km transect and covering seasonal variation at one station. The majority of the investigated species, representing several major bacterioplankton clades, displayed population structures correlating significantly with 1234567890();,: 1234567890();,: environmental factors such as salinity and temperature. Population differentiation was more pronounced over spatial than temporal scales. We discovered genes that have undergone adaptation to different salinity regimes, potentially responsible for the populations’ existence along with the salinity range. This in turn implies the broad existence of ecotypes that may remain undetected by rRNA gene sequencing. Our findings emphasize the importance of physiological barriers, and highlight the role of adaptive divergence as a structuring mechanism of bacterioplankton species. Introduction these studies have demonstrated that 16S rRNA gene clusters (OTUs), or even specific 16S rRNA gene sequences Each liter of seawater contains around a billion bacterial and (amplicon sequence variants; ASVs), represent lineages archaeal cells (bacterioplankton) that play central roles in adapted to different habitats, the 16S rRNA gene does biogeochemical cycles, marine food webs and ecosystem generally not provide sufficient genetic resolution to reveal services [1, 2]. The diversity of aquatic prokaryotes is within-species (intraspecific) diversity patterns, since pro- immense [3]. How this diversity is generated and structured karyotes with identical 16S rRNA gene sequences may have is far from fully understood. Aquatic taxa are differentially highly divergent genomes and phenotypes [9]. distributed among habitats [4] and ribosomal RNA (rRNA) Comparative genomics of isolates, as well as metage- gene sequencing has shown that bacterioplankton commu- nomics on natural samples, have revealed sequence clusters nities are structured both in time and space [5–8]. While of >95% average nucleotide identity (which has emerged as an operational delineation of prokaryotic species [10]); however, it is not known to what extent this intraspecific genomic variation represents neutral diversity vs. adaptation Supplementary information The online version contains to different niches. Due to the technical challenges, rela- supplementary material available at https://doi.org/10.1038/s41396- tively little is known about intraspecific structuring of 021-00985-z. microbes, not least in the marine environment. However, * Anders F. Andersson pioneering studies have shown that genetic content of single [email protected] bacterial species may correlate with geographic distance [11], and that coexisting but ecologically differentiated 1 KTH Royal Institute of Technology, Science for Life Laboratory, Department of Gene Technology, School of Engineering Sciences strains may arise through resource partitioning [12]. For in Chemistry, Biotechnology and Health, Stockholm, Sweden example, the picocyanobacterium Prochlorococcus has fi 2 Åbo Akademi University, Faculty of Science and Engineering, been demonstrated to display ne-scale sequence clusters Environmental and Marine Biology, Åbo, Finland associated with different regimes in temperature and light- Ecologically coherent population structure of uncultivated bacterioplankton 3035 intensity, and single-cell sequencing has revealed distinct on an inbuilt algorithm. While MIDAS and inStrain provide genomic backbones within clusters and variation in acces- genome-wide and gene-specific diversity estimates, sory genes mainly between clusters [13]. The ubiquitous metaSNV reports genome-wide population differentiation and most abundant type of organism in the ocean, the (Manhattan distance). POGENOM outputs both diversity SAR11 clade, has undergone adaptive radiation in response and differentiation parameters, at the whole genome to temperature [14]. Apart from “genome streamlining” (nucleotide diversity and fixation index (FST)) and at the [14, 15], it has been postulated that the ecological success of gene level (nucleotide and amino acid diversity, pN/pS, and this organism is facilitated by its adaptive divergence into FST based on nucleotides and amino acids). POGENOM ecotypes specialized for specific environmental conditions also provides permuted gene-wise FST values, facilitating [6, 16]. However, it is not known if intraspecific niche- significance tests on gene-wise differentiation. differentiation is a general phenomenon in bacterioplankton We here use POGENOM to investigate patterns of or a characteristic of exceptionally abundant species. A genomic variation among a set of bacterioplankton species deeper understanding of intraspecific diversity, sometimes in the Baltic Sea. The Baltic Sea is a geologically young referred to as “microdiversity” [17], is of crucial importance ecosystem with pronounced gradients of salinity, tempera- if we want to understand the ecology, evolution, and spe- ture, and nutrient concentrations, and is often used as a ciation of bacterioplankton, and of prokaryotes in general. model for postglacial colonization and ecological differ- Studying genomic variation within a species can also reveal entiation [27, 28]. Marine macroorganisms display reduced genes involved in adaptation to specific environmental species richness and intraspecific diversity towards the factors, providing new clues on gene functions and cellular northern Baltic Sea, as the lower salinity of these waters mechanisms of adaptation. impose more challenging conditions. Likewise, freshwater The study of metagenomes has been predicted to offer a species diversity decreases with increasing salinity levels more realistic view of prokaryotic diversity [18, 19]as towards the south-west [29]. Moreover, population genetic compared to PCR-based surveys of the 16S rRNA gene. studies have shown that species of fish and macroalgae have Metagenomics offers different routes for addressing intras- distinct genetic populations in the Baltic Proper (central pecific variation. The first is to reconstruct genetic infor- Baltic Sea) compared to the Atlantic west of Sweden [30– mation of individual strains. By mapping reads from one or 32]. With respect to microorganisms, population genetic several samples to the reference genome(s) of a species, the data across the salinity regimes is only available for one gene complement and/or nucleotide sequences at variant eukaryote: the marine diatom Skeletonema marinoi [33]. It positions of the constituent strains can be inferred [20–22]. is evident that the species is locally adapted and genetically This approach is promising, but challenging, especially in differentiated into separate populations on each side of the cases of many coexisting strains. The second approach does Danish Straits, correlating with different salinity regimes not aim at reconstructing strains, but rather uses the reads and oceanographic connectivity. For bacterioplankton, mapped to a reference genome to quantify intra- and community composition has been shown to vary sig- intersample genomic variation of the species. This approach nificantly along the horizontal salinity gradient, as well as is more straightforward for analyzing population structure vertically along oxygen gradients, with the Baltic Proper and works well also in case of highly complex pan- being composed of a mixture of typical freshwater and genomes. Schloissnig et al. [23] conducted pioneering marine taxa [34, 35]. Using metagenomic binning and cross-continental comparative analyses of human gut fragment recruitment analysis, Hugerth et al. [36] showed microbiomes using this approach and showed that there is that the prokaryotic organisms in the Baltic Proper are more intraspecific genetic differentiation between habitats genetically differentiated from closely related marine and (human individuals) than within the same habitat over time. freshwater lineages while displaying high similarity to Similar approaches have been used by Nayfach et al. [11] sequences from North American brackish waters, suggest- and Delmont et al. [24] to show that gene content and amino ing that the Baltic Sea prokaryotes are members of a global acid composition, respectively, differ between oceanic meta-community adapted to brackish conditions. However, regions within individual bacterial species. it remains to be investigated whether the bacterioplankton Here we present the software POGENOM (POpulation species display genetically structured populations within the GENOmics from Metagenomes) that, similarly to MIDAS Baltic Sea ecosystem.
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