Global Habitat Suitability and Ecological Niche Separation in the Phylum Placozoa

<div><p>The enigmatic placozoans, which hold a key position in the metazoan Tree of Life, have attracted substantial attention in many areas of biological and biomedical research. While placozoans have become an emerging model system, their ecology and particularly biogeography remain widely unknown. In this study, we use modelling approaches to explore habitat preferences, and distribution pattern of the placozoans phylum. We provide hypotheses for discrete ecological niche separation between genetic placozoan lineages, which may also help to understand biogeography patterns in other small marine invertebrates. We, here, used maximum entropy modelling to predict placozoan distribution using 20 environmental grids of 9.2 km² resolution. In addition, we used recently developed metrics of niche overlap to compare habitat suitability models of three genetic clades. The predicted distributions range from 55°N to 44°S and are restricted to regions of intermediate to warm sea surface temperatures. High concentrations of salinity and low nutrient concentrations appear as secondary factors. Tests of niche equivalency reveal the largest differences between placozoan clades I and III. Interestingly, the genetically well-separated clades I and V appear to be ecologically very similar. Our habitat suitability models predict a wider latitudinal distribution for placozoans, than currently described, especially in the northern hemisphere. With respect to biogeography modelling, placozoans show patterns somewhere between higher metazoan taxa and marine microorganisms, with the first group usually showing complex biogeographies and the second usually showing “no biogeography.”</p></div

Global maps showing predicted habitat suitability for placozoans based on a 10^th percentile training presence threshold (see text).

<p>Three red, green, and blue colors represent the three placozoan clades, clade I, III and V, respectively. Records with black colors belong to other clades. Yellow represents regions where at least two clades overlap.</p

List of environmental variables used in this study for modelling the global distribution of the phylum Placozoa.

<p>See Tyberghein <i>et al</i> [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0140162#pone.0140162.ref019" target="_blank">19</a>] for full details of layers.</p

Global distribution of placozoans according to Eitel et al. [7] and unpublished data (see the text).

<p>Three red, green, and blue colors represent three investigated clades, clade I, III and V, respectively. Note that the number of localities on the map does not add to 79, because of points overlying in many localities.</p

The phylogram of placozoan haplotypes (species) based on 16S sequences and Bayesian inference (Modified after Eitel et al [7]).

<p>The three clades highlighted in red have been investigated this study.</p

Test AUC values for MaxEnt models of the global distribution for three placozoan clades based on single variable analysis.

<p>Variable values in bold indicate those chosen for final multi-layer models after taking the collinearity values into account. Each column (data sets) uses five different sets of variables.</p

Model evaluation statistics for MaxEnt models of four placozoans data sets (100 replications for each dataset): all-clades, Clade I, Clade III, Clade V.

<p>Model evaluation statistics for MaxEnt models of four placozoans data sets (100 replications for each dataset): all-clades, Clade I, Clade III, Clade V.</p

Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: The placozoan <i>cox1</i> single base pair exon

<div><p>The phylum Placozoa holds a key position for our understanding of the evolution of mitochondrial genomes in Metazoa. Placozoans possess large mitochondrial genomes which harbor several remarkable characteristics such as a fragmented <i>cox1</i> gene and trans-splicing <i>cox1</i> introns. A previous study also suggested the existence of <i>cox1</i> mRNA editing in <i>Trichoplax adhaerens</i>, yet the only formally described species in the phylum Placozoa. We have analyzed RNA-seq data of the undescribed sister species, Placozoa sp. H2 (“Panama” clone), with special focus on the mitochondrial mRNA. While we did not find support for a previously postulated <i>cox1</i> mRNA editing mechanism, we surprisingly found two independent transcripts representing intermediate <i>cox1</i> mRNA splicing stages. Both transcripts consist of partial <i>cox1</i> exon as well as overlapping intron fragments. The data suggest that the <i>cox1</i> gene harbors a single base pair (cytosine) micro exon. Furthermore, conserved group I intron structures flank this unique micro exon also in other placozoans. We discuss the evolutionary origin of this micro exon in the context of a self-splicing intron gain in the <i>cox1</i> gene of the last common ancestor of extant placozoans.</p></div

Placozoan <i>cox1</i> “micro exon” scenario.

<p>The scenario is based on Placozoa sp. H2 “Panama” RNA-seq data. Exon/intron color codes are the same as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177959#pone.0177959.g002" target="_blank">Fig 2</a>. Exon 6¹ represents a truncated exon 6 (following Burger <i>et al</i>., 2009), which is indicated by the superscript 1. Subsequent exons/introns also differ in boundaries and/or numbering from the annotation by Burger <i>et al</i>., 2009 (likewise indicated by a superscript 1). The former intron 6 is now split into two introns (intron 6¹ and 7¹, respectively) flanking the newly identified micro exon 7¹, which has been identified in this study. Splicing of exon 6¹, micro exon 7¹ and exon 8¹ (formerly exon 7, Burger <i>et al</i>., 2009) leads to an in-frame coding sequence (CDS) with the intact CAT triplet coding for the functionally indispensable histidine at the respective position.</p

Mapping of RNA-seq reads on the partial Placozoa sp. H2 "Panama" <i>cox1</i> gene locus containing the micro exon.

<p>The <i>cox1</i> structure is given in the upper part. Exon/intron color codes are the same as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0177959#pone.0177959.g002" target="_blank">Fig 2</a>. Mapping regions I, II and III are indicated by dotted lines and are enlarged below. Reads corresponding to transcript W (comprising exon 6¹, micro exon 7¹ and intron 7¹) span region I and II while reads corresponding to transcript X (comprising intron 6¹, micro exon 7¹ and exon 8¹) span region II and III, respectively. Continuous RNA-seq reads are connected by dashed lines (consequence of the applied gapped mapping procedure).</p