Characterization ofProchlorococcusclades from iron-depleted oceanic regions

Abstract

Prochlorococcus describes a diverse and abundant genus of marine photosynthetic microbes. It is primarily found in oligotrophic waters across the globe and plays a crucial role in energy and nutrient cycling in the ocean ecosystem. The abundance, global distribution, and availability of isolates make Prochlorococcus a model system for understanding marine microbial diversity and biogeochemical cycling. Analysis of 73 metagenomic samples from the Global Ocean Sampling expedition acquired in the Atlantic, Pacific, and Indian Oceans revealed the presence of two uncharacterized Prochlorococcus clades. A phylogenetic analysis using six different genetic markers places the clades close to known lineages adapted to high-light environments. The two uncharacterized clades consistently cooccur and dominate the surface waters of high-temperature, macronutrient-replete, and low-iron regions of the Eastern Equatorial Pacific upwelling and the tropical Indian Ocean. They are genetically distinct from each other and other high-light Prochlorococcus isolates and likely define a previously unrecognized ecotype. Our detailed genomic analysis indicates that these clades comprise organisms that are adapted to iron-depleted environments by reducing their iron quota through the loss of several iron-containing proteins that likely function as electron sinks in the photosynthetic pathway in other Prochlorococcus clades from high-light environments. The presence and inferred physiology of these clades may explain why Prochlorococcus populations from iron-depleted regions do not respond to iron fertilization experiments and further expand our understanding of how phytoplankton adapt to variations in nutrient availability in the ocean.

Global biogeography of Prochlorococcus genome diversity in the surface ocean

“…We also found that sequences mapping to clade c1 (HLIII and HLIV) significantly dominated the Equatorial Pacific Ocean samples (indicator analysis, r.g. = 0.53, P = 0.008) and was consistent with a past analysis of these samples from the region (Rusch et al, 2010). Among HLII clades, c9 (including strain MIT9301) was the most frequent subclade and together with c5, c6 and c7 common across all regions except the California Current, South Atlantic Ocean and Equatorial Pacific Ocean (Supplementary Table S2).…”

“…A set of iron-requiring proteins were frequently under-represented in the Equatorial Pacific Oceanperhaps as an adaptation to lower iron availability (Rusch et al, 2010). In our analysis, we recovered a small subset of these orthologous genes (5 out of the 17 non-core genes) (Rusch et al, 2010) as significantly differentiating between regions.…”

“…In our analysis, we recovered a small subset of these orthologous genes (5 out of the 17 non-core genes) (Rusch et al, 2010) as significantly differentiating between regions. Of these, all were negatively associated with only the Equatorial Pacific Ocean (an Fe-S oxidoreductase and a transglutaminase) or the Equatorial Pacific and other regions (a transglutaminase, a cytochrome oxidase C subunit and a metal-binding protein homologous to CopG-a protein involved in copper homeostasis).…”

“…Within the group, there are multiple phylogenetically distinct lineages and the distribution of this diversity has been linked to environmental factors, such as light, temperature and iron availability (Moore et al, 1998;West and Scanlan, 1999;Johnson et al, 2006;Zwirglmaier et al, 2008;Rusch et al, 2010). It has been suggested that pangenome variability allows Prochlorococcus as a genus to proliferate across many environments (Partensky et al, 1999;Kettler et al, 2007), but it is unclear how the mechanisms of descent contribute to their evolution and the diversity of local populations.…”

“…Metagenomics has also been employed to examine Prochlorococcus genomic diversity at smaller regional scales (Hewson et al, 2009;Rusch et al, 2010;Thompson et al, 2013) but not yet on a global scale. Here we examine the biogeography of Prochlorococcus genome diversity, both in terms of phylogenetic and genome content, globally.…”