Ecology of the rare microbial biosphere of the Arctic Ocean

Abstract

Understanding the role of microbes in the oceans has focused on taxa that occur in high abundance; yet most of the marine microbial diversity is largely determined by a long tail of low-abundance taxa. This rare biosphere may have a cosmopolitan distribution because of high dispersal and low loss rates, and possibly represents a source of phylotypes that become abundant when environmental conditions change. However, the true ecological role of rare marine microorganisms is still not known. Here, we use pyrosequencing to describe the structure and composition of the rare biosphere and to test whether it represents cosmopolitan taxa or whether, similar to abundant phylotypes, the rare community has a biogeography. Our examination of 740,353 16S rRNA gene sequences from 32 bacterial and archaeal communities from various locations of the Arctic Ocean showed that rare phylotypes did not have a cosmopolitan distribution but, rather, followed patterns similar to those of the most abundant members of the community and of the entire community. The abundance distributions of rare and abundant phylotypes were different, following a log-series and log-normal model, respectively, and the taxonomic composition of the rare biosphere was similar to the composition of the abundant phylotypes. We conclude that the rare biosphere has a biogeography and that its tremendous diversity is most likely subjected to ecological processes such as selection, speciation, and extinction.

Fig. 1.

Dendrograms representing the similarity between the composition of 24 bacterial and eight archaeal communities from deep (DAO) and surface (ACB) water masses of the Arctic Ocean. The clustering pattern including all phylotypes is compared with the clustering obtained for abundant phylotypes only (frequency >1%) and for rare phylotypes only (<0.01%). Colors highlight the clusters conserved through the three analyses. Clustering is based on a distance matrix computed with Bray–Curtis similarity. The dendrogram was inferred with the unweighted pair–group average algorithm. Bootstraps values (in percentages) are given at the nodes.

Fig. 2.

Nonmetric multidimensional scaling analysis of the phylotype composition of the abundant (>1%) and rare (<0.01%) bacterial biosphere (n = 48). The analysis separated DAO (deep) from ACB (surface) samples, and the abundant from the rare biosphere. Calculated stress for this analysis using Bray–Curtis similarity = 0.202.

Fig. 3.

Abundance distribution of bacterial and archaeal phylotypes separated as abundant (>1% frequency) and rare (<0.01%). The abundance models predicting the frequency of each abundance class are shown as lines. Abundant phylotypes are predicted by a log-normal model and rare phylotypes by a log-series model. The octaves refer to power-of-2 abundance classes.

Fig. 4.

Venn diagram illustrating the number of bacteria phylotypes being rare in all samples (dark gray) vs. phylotypes always abundant and never rare (white area), and phylotypes being rare in some samples but abundant in others (overlap area).

Fig. 5.

Phylogenetic composition of abundant phylotypes (>1% frequency) compared with rare bacterial phylotypes (<0.01%) in surface (ACB) and deep (DAO) water masses of the Arctic Ocean. NA, not assigned; ns, not significant. *, P < 0.05 (t test results for difference between rare and abundant phylotypes).