Dependence of the Cyanobacterium Prochlorococcus on Hydrogen Peroxide Scavenging Microbes for Growth at the Ocean's Surface

Abstract

The phytoplankton community in the oligotrophic open ocean is numerically dominated by the cyanobacterium Prochlorococcus, accounting for approximately half of all photosynthesis. In the illuminated euphotic zone where Prochlorococcus grows, reactive oxygen species are continuously generated via photochemical reactions with dissolved organic matter. However, Prochlorococcus genomes lack catalase and additional protective mechanisms common in other aerobes, and this genus is highly susceptible to oxidative damage from hydrogen peroxide (HOOH). In this study we showed that the extant microbial community plays a vital, previously unrecognized role in cross-protecting Prochlorococcus from oxidative damage in the surface mixed layer of the oligotrophic ocean. Microbes are the primary HOOH sink in marine systems, and in the absence of the microbial community, surface waters in the Atlantic and Pacific Ocean accumulated HOOH to concentrations that were lethal for Prochlorococcus cultures. In laboratory experiments with the marine heterotroph Alteromonas sp., serving as a proxy for the natural community of HOOH-degrading microbes, bacterial depletion of HOOH from the extracellular milieu prevented oxidative damage to the cell envelope and photosystems of co-cultured Prochlorococcus, and facilitated the growth of Prochlorococcus at ecologically-relevant cell concentrations. Curiously, the more recently evolved lineages of Prochlorococcus that exploit the surface mixed layer niche were also the most sensitive to HOOH. The genomic streamlining of these evolved lineages during adaptation to the high-light exposed upper euphotic zone thus appears to be coincident with an acquired dependency on the extant HOOH-consuming community. These results underscore the importance of (indirect) biotic interactions in establishing niche boundaries, and highlight the impacts that community-level responses to stress may have in the ecological and evolutionary outcomes for co-existing species.

Torn apart and reunited: impact of a heterotroph on the transcriptome of Prochlorococcus

“…Additional transcriptional responses of Prochlorococcus were consistent with a generalized reduction in oxidative stress in the presence of the heterotroph (Morris et al, 2011). For example, multiple DNA repair enzymes, including the DnaJ chaperone, a putative deoxyribodipyrimidine photolyase, the RecG helicase and the error-prone DNA repair protein UmuD were transcriptionally depleted in co-culture (Table 2).…”

“…hlis are found in all Prochlorococcus genomes, but NATL2A is notable for having a much larger suite of hlis than many other Prochlorococcus (Coleman and Chisholm, 2007;Kettler et al, 2007;Berta-Thompson, 2015), which may be related to the ability of this clade of low-light adapted Prochlorococcus to withstand transient exposure to high light intensities (Malmstrom et al, 2010). All 12 of these hli transcripts decreased in relative abundance in co-culture conditions, suggesting that the Alteromonas may have mitigated some form of stress in the culture, such as oxidative stress (Morris et al, 2011). These 'early response' hli transcripts were also found clustered within four sets of adjacent operon-like hli arrays in the genome (arrays 1, 4, 5 and 6; Supplementary Table S2), suggesting that these transcripts may be co-regulated.…”

“…Growth of Prochlorococcus-the numerically dominant phytoplankter in the world's oceans (Flombaum et al, 2013)-in culture is improved by the presence of certain heterotrophs in terms of longevity, stationary phase cell density and ability to grow from low cell density (Sher et al, 2011). This phenomenon is attributable at least in part to the role of heterotrophs in reducing the levels of toxic reactive oxygen species such as hydrogen peroxide (Morris et al, 2008(Morris et al, , 2011. This is thought to compensate for the absence of catalase in the Prochlorococcus genome, indicating that interspecies interactions have clearly influenced the evolutionary selective pressures and processes acting upon this group of organisms (Morris et al, 2012).…”

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

“…Specifically, cysteine and methionine residues are especially sensitive to ROS (Arts et al, 2015). Although heterotrophic bacteria, including some Alteromonas strains, may scavenge ROS and thus reduce potential oxidative stress affecting Prochlorococcus (Morris et al, 2008;Morris et al, 2011), other marine heterotrophic bacteria, again including Alteromonads, in fact produce extracellular superoxide (Diaz et al, 2013). Additionally, the killing mechanism of many antibiotics ultimately involves the generation of ROS (reviewed by Dwyer et al, 2009).…”

“…Several recent studies have shown that co-occurring heterotrophic bacteria can both enhance and inhibit the growth of Prochlorococcus in laboratory co-cultures (Morris et al, 2008;Sher et al, 2011). Furthermore, such interactions may have significant effects on the viability of Prochlorococcus in the oceans, for example through scavenging by heterotrophic bacteria of reactive oxygen species (ROS) produced by Prochlorococcus (Morris et al, 2011(Morris et al, , 2012. Finally, both Prochlorococcus and related Synechococcus strains have been shown to produce a wide diversity of ribosomally-synthesized peptides, which are then post-translationally modified to form lanthipeptides and microcins (Li et al, 2010;Paz-Yepes et al, 2013).…”