Co-culture and biogeography of Prochlorococcus and SAR11

Abstract

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

Ammonia-oxidizing archaea release a suite of organic compounds potentially fueling prokaryotic heterotrophy in the ocean

“…The heterotrophic marine bacterium Pelagibacter ubique , a member of the SAR11 clade, known as the most abundant organisms on the planet 72 , lacks biosynthetic pathways for various vitamins (B 1 , B 5 , B 6 , B 7 , B 12 ) and requires pyruvate, glycine and organic sulphur (e.g., methionine) for growth 73–75 . Recently, it was shown in co-culture experiments that photoautotrophic Prochlorococcus strains can fulfill some of the unique metabolic requirements of SAR11 76 . Additionally, members of the Roseobacter group have been suggested as important suppliers of so-called “public goods” by releasing growth factors as well as biosynthetic precursors, including various vitamin B precursors 27 .…”

Prochlorococcusphage ferredoxin: structural characterization and electron transfer to cyanobacterial sulfite reductases

“…Additionally, some heterotrophs from the Sar11 clade, which constitutes 30% of sea surface bacteria (83), are unable to metabolize sulfate and rely on dissolved reduced sulfur sources (84), potentially those produced by phototrophs, like Prochlorococcus. Conversely, recent work has shown that two ecotypes of P. marinus (MED4 and MIT9313) were unable to supply sufficient reduced sulfur to enable SAR11 growth in laboratory co-cultures (85).…”

Microbial Diversity of Co-occurring Heterotrophs in Cultures of Marine Picocyanobacteria

“…For most of them, including the abundant SAR11 group, high organic carbon conditions present an obstacle (Button, 1991;Cho & Giovannoni, 2004) and hence developing a de ned medium for their growth was a challenge (Carini et al, 2013). Although we designed a medium that sustains co-cultures of SAR11 and Prochlorococcus in log phase (Becker et al, 2019), SAR11 dies precipitously when Prochlorococcus enters stationary phase, suggesting that strict oligotrophs may not be able to tolerate the accumulation of substrates that occur during Prochlorococcus growth -a feature that would have eliminated them in the initial stages of isolating the cyanobacterial strains in our culture collection. This challenge during stationary phase might derive from deleterious effects of high nutrient concentrations on streamlined cellular physiology, with oligotrophs unable to regulate transport rates in the face of high nutrient concentrations (Braakman et al, 2017).…”

“…Abundant, free-living oligotrophic bacteria like Prochlorococcus, many strains of Synechococcus, and members of the SAR11 clade of heterotrophs exhibit genome streamlining, likely driven by reductive evolutionary pressures acting on bacteria that have large population sizes and live in relatively stable environments (Biller, Berube, et al, 2014;Rocap et al, 2003). Together these three groups can represent more than 50% of free-living bacteria in the oligotrophic surface oceans (Becker et al, 2019;Giovannoni, 2017). By contrast, opportunistic marine copiotrophic organisms typically have larger genomes and cell sizes, and are subject to periodic uctuations in abundance, typically depending on an in ux of organic matter for growth (López-Pérez et al, 2012;Romera-Castillo et al, 2011;Tada et al, 2011;Zemb et al, 2010).…”