Cross‐protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities

Abstract

Hydrogen peroxide (HOOH) is a reactive oxygen species, derived from molecular oxygen, that is capable of damaging microbial cells. Surprisingly, the HOOH defence systems of some aerobes in the oxygenated marine environments are critically depleted, relative to model aerobes. For instance, the gene encoding catalase is absent in the numerically dominant photosynthetic cyanobacterium, Prochlorococcus. Accordingly, Prochlorococcus is highly susceptible to HOOH when exposed as pure cultures. Pure cultures do not exist in the marine environment, however. Catalase-positive community members can remove HOOH from the seawater medium, thus lowering the threat to Prochlorococcus and any other member that likewise lacks their own catalase. This cross-protection may constitute a loosely defined symbiosis, whereby the catalase-positive helper cells may benefit through the acquisition of nutrients released by the beneficiaries such as Prochlorococcus. Other members of the community that may be helped by the catalase-positive cells may include some lineages of Synechococcus - the sister genus of Prochlorococcus - as well as some lineages of SAR11 and ammonia oxidizing archaea and bacteria. The co-occurrence of catalase-positive and -negative members suggests that cross-protection from HOOH-mediated oxidative stress may play an important role in the construction of the marine microbial community.

Microbial helpers allow cyanobacteria to thrive in ferruginous waters

“…The well-known extracellular role of KatE on scavenging extracellular H 2 O 2 (Naclerio et al, 1995; Shin, Choi, & Cho, 2008), the presence of KatE in metal-reducing strains, and the link between higher rates of extracellular H 2 O 2 scavenging and growth of cyanobacteria in pre-GOE conditions is suggestive of an important ecological role of KatE in catalase-based interactions, which are thought to be prevalent in the environment (Zinser, 2018). KatE was absent in our model species, Synechococcus spp.…”

“…Similarly, A. macleodii provides catalase as a “public good” to marine Prochlorococcus (Morris et al, 2011) and their KatEs grouped in the first cluster. Alongside nutrient scarcity (Christie-Oleza et al, 2017; Gradoville et al, 2017), protection from toxic byproducts such as ROS toxicity can thus also be an important cooperative ecological mechanism between cyanobacteria and non-phototrophic helpers in modern marine environments (Zinser, 2018), or oceans on early Earth.…”

“…Cooperation occurs when members of a community produce metabolically costly molecules (“public goods”) that become available to neighboring members (Özkaya, Xavier, Dionisio, & Balbontín, 2017). Cooperation is common among cyanobacteria and proteobacteria (Christie-Oleza, Sousoni, Lloyd, Armengaud, & Scanlan, 2017; Zinser, 2018), whose intimate relationship is also evidenced by extensive horizontal gene transfer between the two lineages (Ben Said & Or, 2017; Braakman, Follows, & Chisholm, 2017; Cantine & Fournier, 2017; Cavalier-Smith, 2006a, 2006b; Christie-Oleza et al, 2017; Goldenfeld & Woese, 2011). Cooperation by “helper” organisms providing ROS protection may have also allowed early cyanobacteria to overcome ROS toxicity in Fe 2+ -rich oceans ( Fig.…”

“…Among the heme catalases, monofunctional KatEs originated as clade 2 KatEs and later formed clade 1 and clade 3 (Klotz & Loewen, 2003). Modern proteobacteria can enhance the growth of cyanobacteria by providing ROS protection by secreting catalase (Morris et al, 2011; Zinser, 2018). Extracellular catalases have mostly been found to be of the clade 3 KatE type (Hanaoka et al, 2013; Naclerio, Baccigalupi, Caruso, De Felice, & Ricca, 1995; Pezzoni, Pizarro, & Costa, 2014).…”

Frequency of mispackaging ofProchlorococcusDNA by cyanophage

“…habitat. And finally, other sources of ROS exist in the wild, such as rainfall or the production by other microbes [46], [51] . Thus although mispackaging could be alleviated by the presence of Alteromonas in extremely dense laboratory cultures, this does not mean that it does not occur in the wild.…”