Single‐amplified genomes reveal most streamlined free‐living marine bacteria

Abstract

Evolutionary adaptations of prokaryotes to the environment sometimes result in genome reduction. Our knowledge of this phenomenon among free-living bacteria remains scarce. We address the dynamics and limits of genome reduction by examining one of the most abundant bacteria in the ocean, the SAR86 clade. Despite its abundance, comparative genomics has been limited by the absence of pure cultures and the poor representation in metagenome-assembled genomes. We co-assembled multiple previously available single-amplified genomes to obtain the first complete genomes from members of the four families. All families showed a convergent evolutionary trajectory with characteristic features of streamlined genomes, most pronounced in the TMED112 family. This family has a genome size of ca. 1 Mb and only 1 bp as median intergenic distance, exceeding values found in other abundant microbes such as SAR11, OM43 and Prochlorococcus. This genomic simplification led to a reduction in the biosynthesis of essential molecules, DNA repair-related genes, and the ability to sense and respond to environmental factors, which could suggest an evolutionary dependence on other co-occurring microbes for survival (Black Queen hypothesis). Therefore, these reconstructed genomes within the SAR86 clade provide new insights into the limits of genome reduction in free-living marine bacteria.

Large diversity in the O-chain biosynthetic cluster within populations of Pelagibacterales

“…Furthermore, the term “serotype” should be replaced by “glycotype” which is more realistic (59). In fact, the variation at the level of exposed polysaccharides in microbes belonging to the same population has been revealed by metagenomics, culture, and other approaches as a constant feature, at least, for aquatic microbes (10, 38, 60), including Gram positives (37, 61) and even Archaea (62). The reasons for such extreme flexibility in structures that are often critical to the survival of cells in nature are still obscure, but the most likely explanation is predation or parasitism.…”

Isolate-anchored comparisons reveal evolutionary and functional differentiation across SAR86 marine bacteria

“…A recent publication reported on the assembly of complete SAR86 genomes from collections of closely related SAGs 22 . We attempted to verify the veracity of these assemblies and discovered them to be artificial chimeras resulting from extensive mis-assembly.…”

“…In this study, we provide the first characterization of SAR86 cells in culture and leverage the closed genome sequence of the isolated SAR86 strain in a set of analyses designed to elucidate the evolutionary and functional characteristics of SAR86 bacteria. Despite the ubiquity of SAR86 cells in the global ocean, there is currently little to link extensive 16S rRNA gene-based studies from the past three decades with the genomic diversity uncovered over the past two decades 12,22–25 , and thus no existing backbone from which to interpret relationships between phylogenetic diversity, environmental distribution, and the distribution of functional traits encoded by genomes. Thus, included in our goals were to carefully investigate the HIMB1674 genome along with hundreds of publicly available SAR86 environmental genomes in order to evaluate the evolutionary origins of SAR86 within the Gammaproteobacteria , as well as evolutionary relationships between the strain genome and other SAR86 environmental genomes.…”

“…We used multiple approaches in an attempt to verify that the “complete composite genomes" (CCGs) reported by Roda-Garcia and colleagues are circularized and single contig as reported 10 . First, we attempted to repeat the assembly of CCGs from their respective SAGs using the program Flye v2.9 11 with the arguments ‘-genome size 1.3m -subassemblies’ as reported by Roda-Garcia and colleagues.…”

“…Of the nine assemblies, three were circularized and single contig, one was a single open contig, and six contained multiple contigs (Supplementary Table 1). We also attempted to verify the validity of the nine original CCGs reported by Roda-Garcia et al 10 using a sequence mapping approach. First, we fragmented the original SAGs used to assemble each CCG into 10 kb fragments with 1 kb overlap, and 1 kb fragments with 100 bp overlap, using the tool cut_up_fasta.py from CONCOCT 12 .…”