Ecology of uncultured Prochlorococcus clades revealed through single-cell genomics and biogeographic analysis

Abstract

Prochlorococcus is the numerically dominant photosynthetic organism throughout much of the world’s oceans, yet little is known about the ecology and genetic diversity of populations inhabiting tropical waters. To help close this gap, we examined natural Prochlorococcus communities in the tropical Pacific Ocean using a single-cell whole-genome amplification and sequencing. Analysis of the gene content of just 10 single cells from these waters added 394 new genes to the Prochlorococcus pan-genome—that is, genes never before seen in a Prochlorococcus cell. Analysis of marker genes, including the ribosomal internal transcribed sequence, from dozens of individual cells revealed several representatives from two uncultivated clades of Prochlorococcus previously identified as HNLC1 and HNLC2. While the HNLC clades can dominate Prochlorococcus communities under certain conditions, their overall geographic distribution was highly restricted compared with other clades of Prochlorococcus. In the Atlantic and Pacific oceans, these clades were only found in warm waters with low Fe and high inorganic P levels. Genomic analysis suggests that at least one of these clades thrives in low Fe environments by scavenging organic-bound Fe, a process previously unknown in Prochlorococcus. Furthermore, the capacity to utilize organic-bound Fe appears to have been acquired horizontally and may be exchanged among other clades of Prochlorococcus. Finally, one of the single Prochlorococcus cells sequenced contained a partial genome of what appears to be a prophage integrated into the genome.

Physiology and evolution of nitrate acquisition in Prochlorococcus

“…Nitrate assimilating Prochlorococcus possess a diverse set of nitrogen acquisition pathways Gene content in Prochlorococcus has been shown, for several traits, to reflect the selective pressures in the specific environments from which they (or their genes) were captured Rusch et al, 2007;Coleman and Chisholm, 2010;Feingersch et al, 2012;Malmstrom et al, 2013). Thus, we wondered whether other nitrogen assimilation traits might co-occur with nitrate assimilation in Prochlorococcus, and examined the potential for PAC1, SB and MIT0604 to access alternative sources of nitrogen based on their gene content (Supplementary Table S1 and Supplementary Figure S5).…”

“…Even though individual genomes are small, the collective of all Prochlorococcus cells possesses a vast reservoir of genetic and physiological diversity (Kettler et al, 2007). Prochlorococcus is composed of a polyphyletic group of low-light (LL) adapted clades (LLI-LLVI and NC1), and a more recently diverged monophyletic group of high-light (HL) adapted clades (HLI-HLVI) (Moore et al, 1998;Moore and Chisholm, 1999;Rocap et al, 2002;Martiny et al, 2009c;Lavin et al, 2010;Shi et al, 2011;Huang et al, 2012;Malmstrom et al, 2013). Some of these clades are known to be differentially distributed along gradients of light intensity, temperature and nutrient concentrations (Bouman et al, 2006;Johnson et al, 2006;Zinser et al, 2006;Zwirglmaier et al, 2007Zwirglmaier et al, , 2008Malmstrom et al, 2010Malmstrom et al, , 2013.…”

Transcriptional response of Prochlorococcus to co-culture with a marine Alteromonas: differences between strains and the involvement of putative infochemicals

“…Clade assignment and color coding are according to Kettler et al (2007). Prochlorococcus w7 is a sequenced genome from a single cell sorted from an environmental sample (Malmstrom et al, 2012). Green arrowheads mark the genes shown in (a).…”

Co-occurringSynechococcusecotypes occupy four major oceanic regimes defined by temperature, macronutrients and iron

“…This niche differentiation apparently occurred in a successive or stepwise manner as basal Prochlorococcus clades are better adapted to low-light conditions, a more recently emerged lineage (LLI) can be found throughout the water column, and the most derived clades are high-light adapted. There is evidence of further divergence within the high-light lineage, resulting in ecotypes that occupy different temperature and nutrient regimes (Johnson et al, 2006;Coleman and Chisholm, 2007;Martiny et al, 2009;Malmstrom et al, 2012). Such integration of information about the biogeographic and phylogenetic relatedness of ecotypes provides insight into evolutionary processes underlying niche differentiation in marine microbes.…”