Composition and structure of microbial communities are good indicators of microbial activities and environmental conditions. The evolution of microbial community composition through geological history, therefore, may provide essential clue to the evolution of earth surface environment and its interaction with microbial life. In today’s ocean, coccoidal cyanobacteria take a remarkable portion in planktonic microbes, whereas shallow marine benthic microbial mats are predominantly built by filamentous cyanobacteria. When and how did these two niches occupied by different morphological groups of cyanobacteria remain obscure. Previous studies have proposed a co-evolutionary model between the composition of benthic microbial mats and condition of carbonate substrates in peritidal environments based on geological records from silicified microfossils assemblages in late Mesoproterozoic to early Neoproterozoic strata, with the early stage of this co-evolution not clearly documented. Meanwhile, fossil records of planktonic microbial communities are scarce.

In this study, we present two silicified microfossil assemblages from the early Mesoproterozoic Gaoyuzhuang Formation in North China craton, and the mid-Neoproterozoic Cryogenian Datangpo Formation in South China block, respectively. The Gaoyuzhuang microfossil assemblage contains abundant, delicately preserved microbial mats built by two genera of coccoidal microfossils that colonized on crystal fan layers. In the silicified micritic laminations between the crytal fan and coccoidal mat laminae, there are also clustered filamentous microfossils with some in an upright position, likely a reaction to sediment burial. Unique structures, including coccoidal microfossils attached to and wrapped the filamentous microbes, and stalk-like structure formed by a coccoidal colony, are also found in the fossil assemblage. These findings are interpreted as adaptations of benthic microbial communities to the emergence of marine substrates composed of loose, micritic carbonate sediments, with coccoidal and filamentous microbes colonizing different substrates using different strategies to survive sediment burial. This microbial mat structure may represent an initial stage of the co-evolution process between benthic microbial communities and seafloor conditions.

The Cryogenian Datangpo microfossils contain three types of coccoidal microfossils that are interpreted as representing a cyanobacteria-dominated, planktonic microbial community flourishing in a distal offshore environment. Coccoidal microbes were the major benthic microbial mat builder in Paleoproterozoic when seafloor was covered by chemically precipitated crystal fans, but they retreated from benthic communities in the Neoproterozoic when marine substrates became dominated by micritic sediments according to the co-evolution model between benthic microbial communities and seafloor conditions. The Datangpo microfossil assemblage, therefore, offers a fossil record of planktonic coccoidal microbes during the Cryogenian Period, and suggests that the occupation of the niche of primary producers in open ocean by planktonic coccoidal microbes can be traced back to the Neoproterozoic Era. Together with the Gaoyuzhuang microfossil assemblage, these findings uncover the transition of coccoidal microbes from benthic mat builders to the major planktonic primary producers during the Proterozoic Eon.