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Prochlorococcus and Synechococcus are the two most abundant and widespread phytoplankton in the global ocean. To better understand the factors controlling their biogeography, a reference database of the high-resolution taxonomic marker petB, encoding cytochrome b₆, was used to recruit reads out of 109 metagenomes from the Tara Oceans expedition. An unsuspected novel genetic diversity was unveiled within both genera, even for the most abundant and well-characterized clades, and 136 divergent petB sequences were successfully assembled from metagenomic reads, significantly enriching the reference database. We then defined Ecologically Significant Taxonomic Units (ESTUs)—that is, organisms belonging to the same clade and occupying a common oceanic niche. Three major ESTU assemblages were identified along the cruise transect for Prochlorococcus and eight for Synechococcus. Although Prochlorococcus HLIIIA and HLIVA ESTUs codominated in irondepleted areas of the Pacific Ocean, CRD1 and the yet-to-be cultured EnvB were the prevalent Synechococcus clades in this area, with three different CRD1 and EnvB ESTUs occupying distinct ecological niches with regard to iron availability and temperature. Sharp community shifts were also observed over short geographic distances—for example, around the Marquesas Islands or between southern Indian and Atlantic Oceans—pointing to a tight correlation between ESTU assemblages and specific physico-chemical parameters. Together, this study demonstrates that there is a previously overlooked, ecologically meaningful, fine-scale diversity within some currently defined picocyanobacterial ecotypes, bringing novel insights into the ecology, diversity, and biology of the two most abundant phototrophs on Earth.

The plasticity of bacterial and archaeal genomes makes examining their ecological and evolutionary dynamics both exciting and challenging. The same mechanisms that enable rapid genomic change and adaptation confound current approaches for recovering complete genomes from metagenomes. Here, we use strain-specific patterns of DNA methylation to resolve complex bacterial genomes from long-read metagenomic data of a marine microbial consortium, the “pink berries” of the Sippewissett Marsh (USA). Unique combinations of restriction-modification (RM) systems encoded by the bacteria produced distinctive methylation profiles that were used to accurately bin and classify metagenomic sequences. Using this approach, we finished the largest and most complex circularized bacterial genome ever recovered from a metagenome (7.9 Mb with >600 transposons), the finished genome of Thiohalocapsa sp. PB-PSB1 the dominant bacteria in the consortia. From genomes binned by methylation patterns, we identified instances of horizontal gene transfer between sulfur-cycling symbionts ( Thiohalocapsa sp. PB-PSB1 and Desulfofustis sp. PB-SRB1), phage infection, and strain-level structural variation. We also linked the methylation patterns of each metagenome-assembled genome with encoded DNA methyltransferases and discovered new RM defense systems, including novel associations of RM systems with RNase toxins.

Synechococcus is the second most abundant phytoplanktonic organism on Earth, and its wide genetic diversity allowed it to colonize all the oceans except for polar waters, with different clades colonizing distinct oceanic niches. In recent years, the use of global metagenomics data sets has greatly improved our knowledge of “who is where” by describing the distribution of Synechococcus clades or ecotypes in the open ocean. Marine Synechococcus comprise a numerically and ecologically prominent phytoplankton group, playing a major role in both carbon cycling and trophic networks in all oceanic regions except in the polar oceans. Despite their high abundance in coastal areas, our knowledge of Synechococcus communities in these environments is based on only a few local studies. Here, we use the global metagenome data set of the Ocean Sampling Day (June 21 st , 2014) to get a snapshot of the taxonomic composition of coastal Synechococcus communities worldwide, by recruitment on a reference database of 141 picocyanobacterial genomes, representative of the whole Prochlorococcus , Synechococcus , and Cyanobium diversity. This allowed us to unravel drastic community shifts over small to medium scale gradients of environmental factors, in particular along European coasts. The combined analysis of the phylogeography of natural populations and the thermophysiological characterization of eight strains, representative of the four major Synechococcus lineages (clades I to IV), also brought novel insights about the differential niche partitioning of clades I and IV, which most often co-dominate the Synechococcus community in cold and temperate coastal areas. Altogether, this study reveals several important characteristics and specificities of the coastal communities of Synechococcus worldwide. IMPORTANCE Synechococcus is the second most abundant phytoplanktonic organism on Earth, and its wide genetic diversity allowed it to colonize all the oceans except for polar waters, with different clades colonizing distinct oceanic niches. In recent years, the use of global metagenomics data sets has greatly improved our knowledge of “who is where” by describing the distribution of Synechococcus clades or ecotypes in the open ocean. However, little is known about the global distribution of Synechococcus ecotypes in coastal areas, where Synechococcus is often the dominant phytoplanktonic organism. Here, we leverage the global Ocean Sampling Day metagenomics data set to describe Synechococcus community composition in coastal areas worldwide, revealing striking community shifts, in particular along the coasts of Europe. As temperature appears as an important driver of the community composition, we also characterize the thermal preferenda of 8 Synechococcus strains, bringing new insights into the adaptation to temperature of the dominant Synechococcus clades.

Marine Synechococcus cyanobacteria are major contributors to global oceanic primary production and exhibit a unique diversity of photosynthetic pigments, allowing them to exploit a wide range of light niches. However, the relationship between pigment content and niche partitioning has remained largely undetermined due to the lack of a single-genetic marker resolving all pigment types (PTs). Here, we developed and employed a robust method based on three distinct marker genes (cpcBA, mpeBA, and mpeW) to estimate the relative abundance of all known Synechococcus PTs from metagenomes. Analysis of the Tara Oceans dataset allowed us to reveal the global distribution of Synechococcus PTs and to define their environmental niches. Green-light specialists (PT 3a) dominated in warm, green equatorial waters, whereas blue-light specialists (PT 3c) were particularly abundant in oligotrophic areas. Type IV chromatic acclimaters (CA4-A/B), which are able to dynamically modify their light absorption properties to maximally absorb green or blue light, were unexpectedly the most abundant PT in our dataset and predominated at depth and high latitudes. We also identified populations in which CA4 might be nonfunctional due to the lack of specific CA4 genes, notably in warm high-nutrient low-chlorophyll areas. Major ecotypes within clades I–IV and CRD1 were preferentially associated with a particular PT, while others exhibited a wide range of PTs. Altogether, this study provides important insights into the ecology of Synechococcus and highlights the complex interactions between vertical phylogeny, pigmentation, and environmental parameters that shape Synechococcus community structure and evolution.

Increasing temperatures, with pronounced effects at high latitudes, have raised questions about potential changes in species composition, as well as possible increased importance of small-celled phytoplankton in marine systems. In this study, we mapped out one of the smallest and globally most widespread primary producers, the picocyanobacterium Synechococcus, within the Atlantic inflow to the Arctic Ocean. In contrast to the general understanding that Synechococcus is almost absent in polar oceans due to low temperatures, we encountered high abundances (up to 21,000 cells mL−1) at 79°N, and documented their presence as far north as 82.5°N. Covering an annual cycle in 2014, we found that during autumn and winter, Synechococcus was often more abundant than picoeukaryotes, which usually dominate the picophytoplankton communities in the Arctic. Synechococcus community composition shifted from a quite high genetic diversity during the spring bloom to a clear dominance of two specific operational taxonomic units (OTUs) in autumn and winter. We observed abundances higher than 1000 cells mL−1 in water colder than 2°C at seven distinct stations and size-fractionation experiments demonstrated a net growth of Synechococcus at 2°C in the absence of nano-sized grazers at certain periods of the year. Phylogenetic analysis of petB sequences demonstrated that these high latitude Synechococcus group within the previously described cold-adapted clades I and IV, but also contributed to unveil novel genetic diversity, especially within clade I.

Increasing temperatures, with pronounced effects at high latitudes, have raised questions about potential changes in species composition, as well as possible increased importance of small-celled phytoplankton in marine systems. In this study, we mapped out one of the smallest and globally most widespread primary producers, the picocyanobacterium Synechococcus, within the Atlantic inflow to the Arctic Ocean. In contrast to the general understanding that Synechococcus is almost absent in polar oceans due to low temperatures, we encountered high abundances (up to 21,000 cells mL−1) at 79◦N, and documented their presence as far north as 82.5◦N. Covering an annual cycle in 2014, we found that during autumn and winter, Synechococcus was often more abundant than picoeukaryotes, which usually dominate the picophytoplankton communities in the Arctic. Synechococcus community composition shifted from a quite high genetic diversity during the spring bloom to a clear dominance of two specific operational taxonomic units (OTUs) in autumn and winter. We observed abundances higher than 1000 cells mL−1 in water colder than 2◦C at seven distinct stations and size-fractionation experiments demonstrated a net growth of Synechococcus at 2◦C in the absence of nano-sized grazers at certain periods of the year. Phylogenetic analysis of petB sequences demonstrated that these high latitude Synechococcus group within the previously described cold-adapted clades I and IV, but also contributed to unveil novel genetic diversity, especially within clade I.

Abstract The plasticity of bacterial and archaeal genomes makes examining their ecological and evolutionary dynamics both exciting and challenging. The same mechanisms that enable rapid genomic change and adaptation confound current approaches for recovering complete genomes from metagenomes. Here, we use strain-specific patterns of DNA methylation to resolve complex bacterial genomes from the long-read metagenome of a marine microbial consortia, the “pink berries” of the Sippewissett Marsh. Unique combinations of restriction-modification (RM) systems encoded by the bacteria produced distinctive methylation profiles that accurately binned and classified metagenomic sequences. We linked the methylation patterns of each metagenome-assembled genome with encoded DNA methyltransferases and discovered new restriction modification (RM) defense systems, including novel associations of RM systems with RNase toxins. Using this approach, we finished the largest and most complex circularized bacterial genome ever recovered from a metagenome (7.9 Mb with >600 IS elements), the finished genome of Thiohalocapsa sp. PB-PSB1 the dominant bacteria in the consortia. From these methylation-binned genomes, we identified instances of lateral gene transfer between sulfur-cycling symbionts (Thiohalocapsa sp. PB-PSB1 and Desulfofustis sp. PB-SRB1), phage infection, and strain-level structural variation. Competing Interest Statement Dr. R.J. Roberts works for New England Biolabs, a commercial supplier of restriction enzymes, DNA methyltransferases, and other molecular biology reagents. Drs. Ashby and Heiner work for Pacific Biosciences. Drs. Wilbanks, Dore, and Eisen declare no potential competing interests. Footnotes * Competing Interests: Dr. R.J. Roberts works for New England Biolabs, a commercial supplier of restriction enzymes, DNA methyltransferases, and other molecular biology reagents. Drs. Ashby and Heiner work for Pacific Biosciences. Drs. Wilbanks, Doré, and Eisen declare no potential competing interests. * https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA684324

Bacteria impact humans, industry and nature, but do so under viral constraints. Problematically, knowledge of viral infection efficiencies and outcomes derives from few model systems that over-represent efficient lytic infections and under-represent virus–host natural diversity. Here we sought to understand infection efficiency regulation in an emerging environmental Bacteroidetes –virus model system with markedly different outcomes on two genetically and physiologically nearly identical host strains. For this, we quantified bacterial virus (phage) and host DNA, transcripts and phage particles throughout both infections. While phage transcriptomes were similar, transcriptional differences between hosts suggested host-derived regulation of infection efficiency. Specifically, the alternative host overexpressed DNA degradation genes and underexpressed translation genes, which seemingly targeted phage DNA particle production, as experiments revealed they were both significantly delayed (by >30 min) and reduced (by >50%) in the inefficient infection. This suggests phage failure to repress early alternative host expression and stress response allowed the host to respond against infection by delaying phage DNA replication and protein translation. Given that this phage type is ubiquitous and abundant in the global oceans and that variable viral infection efficiencies are central to dynamic ecosystems, these data provide a critically needed foundation for understanding and modeling viral infections in nature.

Correction to: The ISME Journal (2017) 11, 284–295; doi:10.1038/ismej.2016.81 In the title of the article, 'Bacteriodetes' is misspelled. The proper spelling is 'Bacteroidetes'.

This corrects the article DOI: 10.1038/ismej.2016.81.