Characterization of Prochlorococcus clades 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.

Fig. 1.

Phylogenetic analysis of Prochlorococcus rpsT marker gene. This marker identifies two distinct clades of Prochlorococcus (red and green), each equally divergent from the other two recognized HL clades represented by MED4 and MIT9312 (gold and black). The rpsT (30S ribosomal protein S20) gene from sequenced genomes is shown in bold, whereas those from GOS reads show the site and ID of the containing read. Bootstrap values for neighbor-joining over maximum likelihood approaches are provided as percentages on every branch. Additional markers are presented in Fig. S1.

Fig. 2.

Distribution of Prochlorococcus clades in marine surface water metagenomic samples overlaid on chlorophyll-a measurements. Circles and squares represent sampling sites from Hewson et al. (26) and the GOS (13). Purple, white, and green coloring of the shapes indicates that a site is dominated by the HNLC, eMIT9312, or eMED4 clades, respectively.

Fig. 3.

Canonical correlation analysis showing abundance of Prochlorococcus ecotypes relative to environmental parameters for temperature (actual), iron (modeled), and nitrate (modeled) abundance.