Abstract
Marine picocyanobacteria of the genera Prochlorococcus and Synechococcus are the most abundant photosynthetic organisms on Earth, an ecological success thought to be linked to the differential partitioning of distinct ecotypes into specific ecological niches. However, the underlying processes that governed the diversification of these microorganisms and the appearance of niche-related phenotypic traits are just starting to be elucidated. Here, by comparing 81 genomes, including 34 new Synechococcus, we explored the evolutionary processes that shaped the genomic diversity of picocyanobacteria. Time-calibration of a core-protein tree showed that gene gain/loss occurred at an unexpectedly low rate between the different lineages, with for instance 5.6 genes gained per million years (My) for the major Synechococcus lineage (sub-cluster 5.1), among which only 0.71/My have been fixed in the long term. Gene content comparisons revealed a number of candidates involved in nutrient adaptation, a large proportion of which are located in genomic islands shared between either closely or more distantly related strains, as identified using an original network construction approach. Interestingly, strains representative of the different ecotypes co-occurring in phosphorus-depleted waters (Synechococcus clades III, WPC1, and sub-cluster 5.3) were shown to display different adaptation strategies to this limitation. In contrast, we found few genes potentially involved in adaptation to temperature when comparing cold and warm thermotypes. Indeed, comparison of core protein sequences highlighted variants specific to cold thermotypes, notably involved in carotenoid biosynthesis and the oxidative stress response, revealing that long-term adaptation to thermal niches relies on amino acid substitutions rather than on gene content variation. Altogether, this study not only deciphers the respective roles of gene gains/losses and sequence variation but also uncovers numerous gene candidates likely involved in niche partitioning of two key members of the marine phytoplankton.
Highlights
Understanding how phytoplankton species have adapted to the marine environment, a dynamic system through time and space, is a significant challenge, notably in the context of rapid global change (Edwards and Richardson, 2004; Sears and Angilletta, 2011; Irwin et al, 2015; Doblin and Van Sebille, 2016)
In order to expand the coverage of Synechococcus in available marine picocyanobacterial genomes, 34 new strains were sequenced from cultured isolates, resulting in a quasi-doubling of the current number of complete or near-complete genomes publicly available for this genus
Consistent with the genome streamlining that occurred in most Prochlorococcus lineages (Dufresne et al, 2005, 2008; Kettler et al, 2007), average genome size and GC% are expectedly lower in Prochlorococcus (1.815 Mb and 34.8%, respectively) than in Synechococcus/Cyanobium (2.533 Mb and 59.18%, respectively), with genome sizes ranging from 1.625 Mb for Prochlorococcus HLII strain GP2 to 3.342 Mb for Cyanobium gracile PCC 6307 (SC 5.2) and GC% from 30.8% (EQPAC1, MED4, and MIT9515) to 68.7% (PCC 7001 and PCC 6307, Supplementary Table S1)
Summary
Understanding how phytoplankton species have adapted to the marine environment, a dynamic system through time and space, is a significant challenge, notably in the context of rapid global change (Edwards and Richardson, 2004; Sears and Angilletta, 2011; Irwin et al, 2015; Doblin and Van Sebille, 2016). One of the best ways to better understand these processes is by deciphering the links between current genomic diversity and niche occupancy of these organisms Such an approach requires complete genomes with representatives of distinct ecological niches, a resource which remains limited even with the advent of high-throughput sequencing and the multiplication of partial single amplified genomes (SAGs; Stepanauskas and Sieracki, 2007; Malmstrom et al, 2013; Kashtan et al, 2014; Berube et al, 2019; Nakayama et al, 2019) or metagenomes assembled genomes (MAGs; Iverson et al, 2012; Haro-Moreno et al, 2018). This broad distribution implies that these two microorganisms are able to survive in a large range of environmental niches along in situ gradients of temperature, light intensity as well as micro- and macro-nutrients (Bouman et al, 2006; Zwirglmaier et al, 2008; Scanlan, 2012; Sohm et al, 2015; Farrant et al, 2016)
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