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Ultra-deep sequencing of foraminiferal microbarcodes unveils hidden richness of early monothalamous lineages in deep-sea sediments - PubMed

  • ️Sat Jan 01 2011

Ultra-deep sequencing of foraminiferal microbarcodes unveils hidden richness of early monothalamous lineages in deep-sea sediments

Béatrice Lecroq et al. Proc Natl Acad Sci U S A. 2011.

Abstract

Deep-sea floors represent one of the largest and most complex ecosystems on Earth but remain essentially unexplored. The vastness and remoteness of this ecosystem make deep-sea sampling difficult, hampering traditional taxonomic observations and diversity assessment. This problem is particularly true in the case of the deep-sea meiofauna, which largely comprises small-sized, fragile, and difficult-to-identify metazoans and protists. Here, we introduce an ultra-deep sequencing-based metagenetic approach to examine the richness of benthic foraminifera, a principal component of deep-sea meiofauna. We used Illumina sequencing technology to assess foraminiferal richness in 31 unsieved deep-sea sediment samples from five distinct oceanic regions. We sequenced an extremely short fragment (36 bases) of the small subunit ribosomal DNA hypervariable region 37f, which has been shown to accurately distinguish foraminiferal species. In total, we obtained 495,978 unique sequences that were grouped into 1,643 operational taxonomic units, of which about half (841) could be reliably assigned to foraminifera. The vast majority of the operational taxonomic units (nearly 90%) were either assigned to early (ancient) lineages of soft-walled, single-chambered (monothalamous) foraminifera or remained undetermined and yet possibly belong to unknown early lineages. Contrasting with the classical view of multichambered taxa dominating foraminiferal assemblages, our work reflects an unexpected diversity of monothalamous lineages that are as yet unknown using conventional micropaleontological observations. Although we can only speculate about their morphology, the immense richness of deep-sea phylotypes revealed by this study suggests that ultra-deep sequencing can improve understanding of deep-sea benthic diversity considered until now as unknowable based on a traditional taxonomic approach.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.

Taxonomic composition of deep-sea Foraminifera assemblages based on microbarcode sequences. (A) Proportion of OTUs (solid bars) and reads (hatched bars) for deep-sea samples grouped according to their geographic origins; replicate samples are grouped above dashed lines. (B) Proportion of OTUs (solid bars) and reads (hatched bars) for the whole data set. (C) Proportion of OTUs identified at species (solid colored areas), family-clade (hatched colored areas), and order (solid black areas) level for each foraminiferal order. The numbers above or aside bars indicate the number of OTUs (A and B) or million reads (B). Colors correspond to foraminiferal orders: red, MON; green, ROT; dark blue, TEX; white, ROB; dark green, MIL; blue, SPI; pink, GLO.

Fig. 2.
Fig. 2.

Phylogenetic diversity of assigned OTUs based on ML analysis of corresponding partial SSU rDNA sequences. The unresolved lineages leaf includes monothalamids sequences that could not be confidently placed in any of illustrated clades. Horizontal bars represent the number of OTUs corresponding to each clade. Sequences identified up to the order-level only (MON) were not included. Bootstraps of 95% or more are indicated. Colors correspond to foraminiferal orders as in Fig. 1.

Fig. 3.
Fig. 3.

Cosmopolitanism patterns in deep-sea foraminiferal OTUs. (A) Relative abundance of the 10 most sequenced CosmoOTUs across the five geographic zones. Proportion of reads is indicated by circle size. Each circle in a cluster corresponds to a CosmoOTU, in decreasing order of reads abundance (from 1 to 10). (B) Proportions of reads and OTUs exclusively recovered in two, three, four, or five different geographic zones. (C) Proportions of order-level taxa found in two, three, four, or five different geographic zones. Total numbers of OTUs are indicated. Colors correspond to foraminiferal orders as in Fig. 1.

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