Ultrarare marine microbes contribute to key sulphur-related ecosystem functions

Abstract

The description of a rare biosphere within microbial communities has created great interest because microbes play a fundamental role in the functioning of all ecosystems on earth. Despite recent progress in understanding the ecology of the rare biosphere, the concept itself is still discussed, and fundamental questions remain. Here, we target the seed bank compartment of the rare biosphere, assess the level of rarity at which micro-organisms are still able to colonize an ecosystem and investigate whether rare species are functionally redundant. Using an original experimental design where wood in aquaria was inoculated with increasingly diluted coastal seawater, we show that bacteria that represented as few as 0.00000002% of the cells in the environment (or 1 cell in 10 L of seawater) were still able to grow and play key roles within the ecosystem. Our experiment further showed that some bacteria can be replaced by others that have the potential to fulfil the same metabolic tasks. This finding suggests some functional redundancy within bacterial species. However, when ultrarare bacteria were progressively removed, productivity was reduced, and below a certain threshold some processes were lost, and the function of the ecosystem was altered. Overall the study shows that bacteria that are not detected by high-throughput sequencing approaches are nevertheless viable and able to colonize new ecosystems, suggesting the need to consider ultrarare microbes in the marine environment.

Keywords: bacteria; colonization; diversity; functional redundancy; rare biosphere; succession; sulphide; sulphur cycle.