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Ecology of the Rare Microbial Biosphere of the Arctic Ocean

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Ecology of the Rare Microbial Biosphere of the Arctic Ocean Ecology of the rare microbial biosphere of the Arctic Ocean Pierre E. Galanda,b,c,1, Emilio O. Casamayora, David L. Kirchmand, and Connie Lovejoye aDepartment of Continental Ecology-Limnology, Centre d’Estudis Avanc¸ats de Blanes–CSIC, Blanes, Spain; dSchool of Marine Science and Policy, University of Delaware, Lewes, DE 19958; eQue´bec-Oce´an, De´partement de Biologie, and Institut de Biologie Inte´grative et des Syste`mes, Universite´Laval, Que´bec, QC, Canada G1V 0A6; and bUPMC, Univ Paris 06 and cCNRS, UMR 7621, LOBB, Observatoire Océanologique, F-66651, Banyuls/mer, France Edited by David M. Karl, University of Hawaii, Honolulu, HI, and approved October 28, 2009 (received for review July 23, 2009) Understanding the role of microbes in the oceans has focused on taxa is the most studied part of the community. The other component, that occur in high abundance; yet most of the marine microbial named ‘‘the rare biosphere’’ (11), comprises a very high number of diversity is largely determined by a long tail of low-abundance taxa. rare species that contains most of the diversity (2). The presence of This rare biosphere may have a cosmopolitan distribution because of this long tail of rare microbes was first demonstrated by targeted high dispersal and low loss rates, and possibly represents a source of pyrosequencing of marine bacteria in the deep Atlantic (11), then phylotypes that become abundant when environmental conditions in deep oceanic vents (8) and in the Arctic Ocean both for bacteria change. However, the true ecological role of rare marine microor- (12, 13) and archaea (7). ganisms is still not known. Here, we use pyrosequencing to describe As accumulating data confirm the prevalence of the rare bio- the structure and composition of the rare biosphere and to test sphere, we still know little about its ecological and functional role whether it represents cosmopolitan taxa or whether, similar to in the ocean. The main hypothesis proposes that the rare members abundant phylotypes, the rare community has a biogeography. Our of the biosphere have a cosmopolitan distribution because of a low examination of 740,353 16S rRNA gene sequences from 32 bacterial loss rate by viral lysis or predation, combined with potentially and archaeal communities from various locations of the Arctic Ocean unlimited dispersal capacity governed by stochastic immigration showed that rare phylotypes did not have a cosmopolitan distribu- (2). The goal of this study was thus to test whether the rare tion but, rather, followed patterns similar to those of the most biosphere represents cosmopolitan taxa or whether, similar to abundant members of the community and of the entire community. abundant phylotypes, the rare community has a biogeography The abundance distributions of rare and abundant phylotypes were structured by ecological processes such as selection and speciation. different, following a log-series and log-normal model, respectively, We used data from 16S rRNA gene pyrosequencing analysis of 24 and the taxonomic composition of the rare biosphere was similar to bacterial and eight archaeal samples from across the Arctic Ocean the composition of the abundant phylotypes. We conclude that the to compare the similarity among rare members of the communities. rare biosphere has a biogeography and that its tremendous diversity We furthermore applied models for abundance distribution and is most likely subjected to ecological processes such as selection, described the taxonomic composition of both rare and abundant speciation, and extinction. phylotypes. Results abundance distribution ͉ bacteria ͉ archaea ͉ pyrosequencing ͉ biogeography Similarity Among Communities. We assessed the community simi- larity among sites by comparing the relative abundance and distri- bution of 545,246 bacterial and 195,107 archaeal V6 tag 16S rRNA arine microbes are essential for the functioning of marine gene sequences (Table S1). We separated the microbial phylotypes Mecosystems (1), yet the extent of their diversity remains (defined in Materials and Methods) as abundant or rare. Rare unclear (2). The early approach of direct cultivation to identify phylotypes were arbitrarily defined as having a frequency Ͻ0.01% marine microbes gave very low estimates of diversity and abun- and abundant phylotypes a frequency Ͼ1% within a sample. Our dance. The development and in situ application of molecular tools data showed that the grouping for the rare bacterial phylotypes was greatly changed our perception of microbial diversity, revealing that similar to the clustering of the abundant phylotypes, which in turn only a very small fraction of microorganisms were detected by was similar to the clustering of the entire community (Fig. 1). culture (3). These cultivation-independent approaches showed that Archaeal communities gave the same result (Fig. 1). Cluster microbes represent the main diversity of life on earth (4). In marine analysis separated the communities into two main groups. One systems, the diversity of microbes seems to increase with increasing group contained all communities from surface waters (samples sampling effort and resolving power of new molecular tools. ACB, Fig. 1), and the other group contained all deep water mass MICROBIOLOGY Initially the diversity of marine bacteria was predicted to be as low communities (samples DAO). Deep communities were further as a few thousand taxa (5); more recent estimates have raised the separated into two clusters. One cluster contained communities 6 9 number to 10 –10 taxa (2). The diversity of archaea, in turn, from the Eurasian Basin (colored red in Fig. 1), and the other appears generally to be much lower than for bacteria (6), and cluster contained communities from the Canada Basin (blue) of the marine archaea could be 5–10 times less diverse than bacteria (7, 8). Arctic Ocean. Surface samples separated into three groups. The The main focus of marine molecular microbial studies has been first group comprised samples collected mostly in winter with three on the most abundant members of the communities for practical from January, but with one sample from July (cluster colored black, reasons; the abundant phylotypes are the easiest to detect with the most widely used molecular tools. PCR-based fingerprinting and cloning techniques using universal primers most easily amplify Author contributions: P.E.G., D.L.K., and C.L. designed research; P.E.G. performed research; microbes with abundances in the ecosystem of Ͼ1% of the total P.E.G. analyzed data; and P.E.G., E.O.C., D.L.K., and C.L. wrote the paper. community (2, 9). The most abundant taxa are also thought to be The authors declare no conflict of interest. the most active and most important in fluxes of dissolved organic This article is a PNAS Direct Submission. matter (10). However, abundant species represent only a small Freely available online through the PNAS open access option. portion of microbial diversity. Analyses of abundance distribution 1To whom correspondence should be addressed. E-mail: [email protected]. indicate that diversity is divided into two main components. One This article contains supporting information online at www.pnas.org/cgi/content/full/ component includes the few species that are very abundant, which 0908284106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0908284106 PNAS ͉ December 29, 2009 ͉ vol. 106 ͉ no. 52 ͉ 22427–22432 Downloaded by guest on September 29, 2021 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 Ͼ1%) and for rare phylotypes only (Ͻ0.01%). 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. 1). The second contained only summer samples collected in Nonmetric multidimensional scaling analysis showed that the July and August (cluster in green) and the third cluster contained rare phylotypes better separated ACB samples (surface) from DAO two July and one January sample (cluster in yellow). Archaea samples (deep waters) than the abundant phylotypes did (Fig. 2). separated into three main groups. One contained all surface This analysis also revealed that the difference in community samples (red, Fig. 1), the other all deep water samples (blue), and composition was greater between rare and abundant phylotypes the third only one sample (black). This grouping was similar for the than between surface and deep samples. The result was the same abundant and rare samples (the single exception being sample when the more stringent definition (100%) of a phylotype was used ACB࿝0015). (Fig. S3). When phylotypes were defined more stringently (100% identity), the community grouping was still similar between rare and abun- Rare and Abundant Phylotypes. There was a clear difference be- dant phylotypes for both bacteria and archaea (Fig. S1). The tween the abundance distributions of the rare and abundant patterns of biogeography were still present for rare phylotype with phylotypes (Fig. 3). The rare phylotypes followed a log-series a frequency Ͻ0.001% (Fig. S2). Such a low frequency could be distribution, whereas the abundant phylotypes
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