Vampires in the oceans: predatory cercozoan amoebae in marine habitats

Abstract

Vampire amoebae (vampyrellids) are predators of algae, fungi, protozoa and small metazoans known primarily from soils and in freshwater habitats. They are among the very few heterotrophic naked, filose and reticulose protists that have received some attention from a morphological and ecological point of view over the last few decades, because of the peculiar mode of feeding of known species. Yet, the true extent of their biodiversity remains largely unknown. Here we use a complementary approach of culturing and sequence database mining to address this issue, focusing our efforts on marine environments, where vampyrellids are very poorly known. We present 10 new vampyrellid isolates, 8 from marine or brackish sediments, and 2 from soil or freshwater sediment. Two of the former correspond to the genera Thalassomyxa Grell and Penardia Cash for which sequence data were previously unavailable. Small-subunit ribosomal DNA analysis confirms they are all related to previously sequenced vampyrellids. An exhaustive screening of the NCBI GenBank database and of 454 sequence data generated by the European BioMarKs consortium revealed hundreds of distinct environmental vampyrellid sequences. We show that vampyrellids are much more diverse than previously thought, especially in marine habitats. Our new isolates, which cover almost the full phylogenetic range of vampyrellid sequences revealed in this study, offer a rare opportunity to integrate data from environmental DNA surveys with phenotypic information. However, the very large genetic diversity we highlight within vampyrellids (especially in marine sediments and soils) contrasts with the paradoxically low morphological distinctiveness we observed across our isolates.

Vernalophrys algivore gen. nov., sp. nov. (Rhizaria: Cercozoa: Vampyrellida), a New Algal Predator Isolated from Outdoor Mass Culture of Scenedesmus dimorphus

“…8) (90% and 0.95 by ML and BI). Similar to the study of Berney et al (24), three main clades (A, B, and C) of vampyrellids were recovered (Fig. 8).…”

“…8) and was close to the members of the Leptophryidae, such as Arachnula, Theratromyxa, and Platyreta. Our vampyrellid grouped with two environmental cercozoan isolates from anoxic sediments (24) with bootstrap values of 57% and 0.96 (ML/BI).…”

“…Distribution and environmental considerations. As predators of algae, fungi, protozoa, and small metazoa, vampyrellids are common in soils, freshwater and marine water columns, and sediments and are suspected to have a significant role in microbial ecosystems (24,46). However, little is known about their distribution in large-scale algal cultures in which plenty of prey algae are available.…”

“…They generally occur in soils and freshwater (14,20), but some have been detected in marine habitats (24). Three further genera of filose algivorous amoebae have been reported, but one (Vampyrellidium, Zopf 1885) is related to the nucleariid filose amoebae, and the affinities of the other two (Asterocaelum, Canter 1973 and Hyalodiscus, Hertwig and Lesser 1874) have yet to be resolved.…”

Tiny vampires in ancient seas: evidence for predation via perforation in fossils from the 780–740 million-year-old Chuar Group, Grand Canyon, USA

“…In support of this view, the holes are similar to those made by modern predatory protists that perforate the resistant walls of their prey to consume the cell contents inside. This 'vampire-like' behaviour is widespread among eukaryotes, occurring in, for example, the amoeboid trophic phases of some amoebozoan slime moulds [24]; several close relatives of the Fungi [25,26]; the foraminiferan Floresina amphiphaga [27]; and several different cercozoan clades [28][29][30][31]. (Note that the term parasite has been applied to some of these organisms because they insert themselves fully inside the wall of the 'host' cell, consuming it from within [26].…”