A strong link between marine microbial community composition and function challenges the idea of functional redundancy

Abstract

Marine microbes have tremendous diversity, but a fundamental question remains unanswered: why are there so many microbial species in the sea? The idea of functional redundancy for microbial communities has long been assumed, so that the high level of richness is often explained by the presence of different taxa that are able to conduct the exact same set of metabolic processes and that can readily replace each other. Here, we refute the hypothesis of functional redundancy for marine microbial communities by showing that a shift in the community composition altered the overall functional attributes of communities across different temporal and spatial scales. Our metagenomic monitoring of a coastal northwestern Mediterranean site also revealed that diverse microbial communities harbor a high diversity of potential proteins. Working with all information given by the metagenomes (all reads) rather than relying only on known genes (annotated orthologous genes) was essential for revealing the similarity between taxonomic and functional community compositions. Our finding does not exclude the possibility for a partial redundancy where organisms that share some specific function can coexist when they differ in other ecological requirements. It demonstrates, however, that marine microbial diversity reflects a tremendous diversity of microbial metabolism and highlights the genetic potential yet to be discovered in an ocean of microbes.

Fig. 1

Similarity in functional attributes is related to similarity in community composition and shows reproducible patterns over time. a The relationship between the similarity in communities’ overall functional attributes and community composition (R² = 0.8, P < 0.001, F test for the overall significance of the linear regression). b Pairwise comparisons of the overall functional attributes for communities sampled during a 3-year period at the SOLA station in the coastal northwest Mediterranean Sea. The similarity in functional attributes was measured by a direct metagenome-to-metagenome comparison of the sequence content, which gave results similar to the ones obtained by using all predicted proteins (Supplementary Fig. S3). The similarity between communities (1- Bray-Curtis dissimilarity) was estimated from the composition of 16S rRNA genes

Fig. 2

The similarity in overall community functional attributes and community composition in the Mediterranean Sea (a) and Atlantic Ocean (b). All communities were sampled during the 2014 summer solstice. The similarity in overall community functional attributes was measured by a direct metagenome-to-metagenome comparison of the sequence content. The similarity between communities (1- Bray-Curtis dissimilarity) was estimated from the composition of 16S rRNA genes

Fig. 3

The seasonal structure of the microbial communities. a The structure of the overall community functional attributes across different seasons. b The structure of the microbial community composition across different seasons. The nonmetric multidimensional scaling plots are based on a Bray-Curtis dissimilarity calculated from the composition of all predicted proteins (a) or the composition of 16S rRNA genes (b)

Fig. 4

Functional processes during the year at the SOLA station in the coastal northwest Mediterranean Sea. The processes showing a proportion of genes with significant differences across seasons are shown. Genes were annotated against the KEGG database

Fig. 5

The community richness compared to the functional richness. The taxonomic richness was based on the number of OTUs detected in the communities and the functional richness was based on the total number of predicted proteins found in the communities.