Heterokont Predator Develorapax marinus gen. et sp. nov. - A Model of the Ochrophyte Ancestor.

Vladimir V Aleoshin,Gulnara S Mirzaeva,Alexander P Mylnikov,Kirill V Mikhailov,Sergey A Karpov

doi:10.3389/fmicb.2016.01194

Abstract

Heterotrophic lineages of Heterokonta (or stramenopiles), in contrast to a single monophyletic group of autotrophs, Ochrophyta, form several clades that independently branch off the heterokont stem lineage. The nearest neighbors of Ochrophyta in the phylogenetic tree appear to be almost exclusively bacterivorous, whereas the hypothesis of plastid acquisition by the ancestors of the ochrophyte lineage suggests an ability to engulf eukaryotic alga. In line with this hypothesis, the heterotrophic predator at the base of the ochrophyte lineage may be regarded as a model for the ochrophyte ancestor. Here, we present a new genus and species of marine free-living heterotrophic heterokont Develorapax marinus, which falls into an isolated heterokont cluster, along with the marine flagellate Developayella elegans, and is able to engulf eukaryotic cells. Together with environmental sequences D. marinus and D. elegans form a class-level clade Developea nom. nov. represented by species adapted to different environmental conditions and with a wide geographical distribution. The position of Developea among Heterokonta in large-scale phylogenetic tree is discussed. We propose that members of the Developea clade represent a model for transition from bacterivory to a predatory feeding mode by selection for larger prey. Presumably, such transition in the grazing strategy is possible in the presence of bacterial biofilms or aggregates expected in eutrophic environment, and has likely occurred in the ochrophyte ancestor.

Highlights

Heterokonta is one of the major groups of eukaryotes and encompasses organisms with a wide variety of life styles – from autotrophic diatom algae and kelps to heterotrophic bicosoecid flagellates and parasitic oomycetes
The result of molecular phylogenetic analysis with small and large subunit rRNA gene sequences confirms that Develorapax marinus and Developayella elegans are sisters
D. marinus differs from D. elegans in the details of morphology and biological peculiarities, which justifies its description as a new genus and species

Summary

Introduction

Heterokonta is one of the major groups of eukaryotes and encompasses organisms with a wide variety of life styles – from autotrophic diatom algae and kelps to heterotrophic bicosoecid flagellates and parasitic oomycetes. Heterotrophic lineages of heterokonts do not form a single group, and are instead found as several clades that branch off the heterokont stem lineage preceding the divergence of ochrophytes (Leipe et al, 1994, 1996; Riisberg et al, 2009; Yubuki et al, 2010, 2015). Among recent heterotrophic and mixotrophic species there are those that are able to consume both bacterial and eukaryotic prey (Strom, 1991; Burkholder et al, 2008; Piwosz and Pernthaler, 2010; Zhang et al, 2013; Lee et al, 2014; Mitra et al, 2016) while others are limited by the size of prey cells, with some eukaryotes lacking the ability to graze on bacteria (Jonsson, 1986; Hansen and Calado, 1999; Montagnes et al, 2008). Flagellates, adhering to the second strategy, are able to consume bacterial biofilms, including those that grow on solid substrates (Böhme et al, 2009; Erken et al, 2012)

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