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.

Temperate and tropical coastal waters share relatively similar microbial biofilm communities while free‐living or particle‐attached communities are distinct

“…Therefore, a higher frequency of sampling effort could also help to associate biofilm OTUs to rare FL OTUs. However, even if not detected in high‐throughput sequencing, ultrarare microorganisms are able to colonize new surfaces (Kalenitchenko et al, 2018).…”

Historical contingency impacts on community assembly and ecosystem function in chemosynthetic marine ecosystems

“…In addition, our study takes a step further by gathering data from a marine ecosystem where the effect of historical contingencies is shown to be transient. The microorganisms that colonize wood in seawater are considered to be ultra-rare members of the planktonic microbial community 26 . They probably remain inactive or dormant in seawater until they encounter a favorable substrate that they can colonize.…”

“…The wood was not autoclaved to avoid altering the integrity of the chemical composition (possible impact on sugars and lipids). However, few bacteria are found naturally in living wood, and a previous experiment showed no rDNA amplification of terrestrial microbes following immersion in seawater, which induces an osmotic shock for the microbial cells 26 . All aquaria were equipped with a diffusor connected to an air compressor to ensure continuous oxygen saturation of the water.…”

“…The four identical cores were taken along a same growth ring 2 cm from the bark. Four replicate cores per sampling interval provide the necessary coverage of the micro variability of the wood 26 . It was preferable to sample four cores from the same removed log instead of drilling one core per immerged wood log to reduce the risk of influencing the wood's redox gradient.…”

“…To answer this question, an experimental approach that monitors historical contingencies and current environmental conditions was needed 6 . We already showed that wood incubated in seawater is a useful tool for testing hypotheses on the functional ecology of communities 25,26 . Here, wood logs incubated in aquaria were inoculated with sea water microbes from either surface or deep waters.…”