Interactions between marine cyanobacteria and heterotrophic bacteria: A case study of <italic>Prochlorococcus</italic>

Abstract

Cyanobacteria are the key primary producers in the global ocean and account for 25% of its net productivity. They play a vital role in the ocean by driving the circulation of matter and the flow of energy via the absorption of considerable amounts of carbon dioxide and the release of dissolved organic matter. This dissolved organic matter is converted into biomass by marine heterotrophs, which keeps the cycling of elements in oligotrophic waters at equilibrium. Prochlorococcus, an ecologically important genus of cyanobacteria, is the smallest and most abundant oxygenic phototroph in the global ocean. Prochlorococcus has highly streamlined genomes, which can provide a competitive advantage in the oligotrophic surface waters; however, the streamlined genomes also force Prochlorococcus to adapt to a narrow range of environmental parameters. Owing to these genomic characteristics, Prochlorococcus often establishes interactions with heterotrophic bacteria to survive in the challenging marine environment. Because cyanobacteria are abundant in the ocean, the cyanobacteria-heterotrophic bacteria relationship can significantly affect marine carbon sequestration and storage, which in turn has important ecological implications. Previous studies have reported on the relationships between Prochlorococcus and various heterotrophic bacteria. For example, Prochlorococcus establishes positive interactions with Alteromonas sp. that enhance its growth rate and environmental adaptability . In this review, we discuss the underlying mechanisms of the interaction patterns between Prochlorococcus and heterotrophic bacteria, as well as their genetic, physiological, and ecological significance. Prochlorococcus and heterotrophic bacteria tend to form mutualistic relationships in which they directly or indirectly exchange metabolites or recycle organic carbon through complementary excretion and crosstalk between pathways, such as citrate, glycolate, and malate pathways. Prochlorococcus and heterotrophic bacteria also commonly establish commensal relationships. For instance, heterotrophic bacteria protect Prochlorococcus by scavenging hydrogen peroxide, which Prochlorococcus is sensitive to. Although many heterotrophic bacteria cannot synthesize vitamin B12, they require it as a cofactor for essential functions. Their genetic characteristics suggest that most cyanobacteria have the pathways for synthesizing vitamin B12, but that they may provide vitamin B12 to heterotrophic bacteria to promote the growth of “helper” in the oligotrophic ocean. Therefore, the interactions between cyanobacteria and heterotrophic bacteria help maintain the stability and diversity of marine ecosystems. Global climate change may influence cyanobacteria-heterotrophic bacteria interactions, which could directly affect the structure and dynamics of the microbial community in the oligotrophic ocean, and therefore, primary productivity and element cycling in the ocean. Here, we suggest future research priorities and potential applications based on newfound knowledge of the subject. First, using the known “heterotrophic bacteria-cyanobacteria” relationships, the cultivation of marine heterotrophic bacteria, cyanobacteria and their viruses should be promoted to build a more comprehensive “cyanobacteria-heterotrophic bacteria-virus” ecological model for marine environments. Second, the interaction mechanisms between cyanobacteria and heterotrophic bacteria should be revealed by new biotechnologies, such as (meta) genomics, (meta) transcriptomics, (meta) proteomics, and (meta) metabolomics.Third, cyanobacteria-heterotrophic bacteria interactions should be studied against the backdrop of climate change using both ex situ (i.e., laboratory) and in situ investigations to predict changes in marine microbial community and its potential impact on biogeochemical cycling in oceans.