Microbial helpers allow cyanobacteria to thrive in ferruginous waters

Abstract

The Great Oxidation Event (GOE) was a rapid accumulation of oxygen in the atmosphere as a result of the photosynthetic activity of cyanobacteria. This accumulation reflected the pervasiveness of O2 on the planet's surface, indicating that cyanobacteria had become ecologically successful in Archean oceans. Micromolar concentrations of Fe2+ in Archean oceans would have reacted with hydrogen peroxide, a byproduct of oxygenic photosynthesis, to produce hydroxyl radicals, which cause cellular damage. Yet, cyanobacteria colonized Archean oceans extensively enough to oxygenate the atmosphere, which likely required protection mechanisms against the negative impacts of hydroxyl radical production in Fe2+‐rich seas. We identify several factors that could have acted to protect early cyanobacteria from the impacts of hydroxyl radical production and hypothesize that microbial cooperation may have played an important role in protecting cyanobacteria from Fe2+ toxicity before the GOE. We found that several strains of facultative anaerobic heterotrophic bacteria (Shewanella) with ROS defence mechanisms increase the fitness of cyanobacteria (Synechococcus) in ferruginous waters. Shewanella species with manganese transporters provided the most protection. Our results suggest that a tightly regulated response to prevent Fe2+ toxicity could have been important for the colonization of ancient ferruginous oceans, particularly in the presence of high manganese concentrations and may expand the upper bound for tolerable Fe2+ concentrations for cyanobacteria.

An overview of experimental simulations of microbial activity in early Earth

“…It is therefore important to understand the forcings for primary productivity in early Earth. Several experimental studies have been conducted to investigate the response of primary productivity to Precambrian conditions, such as high seawater Fe(II), high atmospheric p CO 2 , and unique ecophysiological mechanisms such as competition for nutrients between oxygenic cyanobacteria and Fe(II)-oxidising anoxygenic photosynthesizers ( Swanner et al, 2015 ; Kamennaya et al, 2018 ; Ozaki et al, 2019 ; Herrmann et al, 2021 ; Szeinbaum et al, 2021 ). Although extant organisms used in the studies described almost certainly cannot be mapped to those present in ecosystems on the early Earth, we can reasonably assume that their core metabolic pathways and ecological activities had equivalents in those early ecosystems (e.g., Falkowski et al, 2008 ).…”

“…However, several lines of evidence show that Fe(II) toxicity might have not significantly limited the expansion of cyanobacteria in the early oceans ( Ward et al, 2019 ; Szeinbaum et al, 2021 ). Firstly, many types of terrestrial cyanobacteria can survive at high Fe(II) concentrations (10–150 μM), which characterised the Archean oceans ( Brown et al, 2005 ; Thompson et al, 2019 ; Ward et al, 2019 ).…”

“…Firstly, many types of terrestrial cyanobacteria can survive at high Fe(II) concentrations (10–150 μM), which characterised the Archean oceans ( Brown et al, 2005 ; Thompson et al, 2019 ; Ward et al, 2019 ). Next, microbial “helpers” such as facultative anaerobic gammaproteobacterial Shewanella using an ROS defence strategy, might have partially relieved the toxicity of Fe(II) on cyanobacteria ( Szeinbaum et al, 2021 ). This is because the Fe(II) toxicity of cyanobacteria could be generated by the hydroxyl radicals from the reaction between Fe(II) and ROS formed during photosynthesis ( Swanner et al, 2015 ; Szeinbaum et al, 2021 ).…”

“…Next, microbial “helpers” such as facultative anaerobic gammaproteobacterial Shewanella using an ROS defence strategy, might have partially relieved the toxicity of Fe(II) on cyanobacteria ( Szeinbaum et al, 2021 ). This is because the Fe(II) toxicity of cyanobacteria could be generated by the hydroxyl radicals from the reaction between Fe(II) and ROS formed during photosynthesis ( Swanner et al, 2015 ; Szeinbaum et al, 2021 ). Finally, experimental setup and strain selection may have a great influence on the conclusion ( Herrmann et al, 2021 ).…”

“…Meanwhile, the effect of a single species may not be applicable to an entire ecosystem. This is due to the existence of competition and mutualistic symbiosis in the ecosystem (e.g., Ozaki et al, 2019 ; Szeinbaum et al, 2021 ), which could significantly alter the adaptability of microorganisms to certain environments. Experimental studies on microbial mats usually include the entire microbial ecosystem.…”