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The Phylogenetic Position of the Oxymonad Saccinobaculus Based on SSU Rrna

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The Phylogenetic Position of the Oxymonad Saccinobaculus Based on SSU Rrna ARTICLE IN PRESS Protist, Vol. ], ]]]—]]], ]] ]]]] http://www.elsevier.de/protis Published online date 10 July 2006 ORIGINAL PAPER The Phylogenetic Position of the Oxymonad Saccinobaculus Based on SSU rRNA Aaron A. Heiss, and Patrick J. Keeling1 Botany Department, Canadian Institute for Advanced Research, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, Canada V6 T 1Z4 Submitted April 12, 2006; Accepted May 30, 2006 Monitoring Editor: Michael Melkonian The oxymonads are a group of structurally complex anaerobic flagellates about which we know very little. They are found in association with complex microbial communities in the guts of animals. There are five recognized families of oxymonads; molecular data have been acquired for four of these. Here, we describe the first molecular data from the last remaining group, represented by Saccinobaculus, an organism that is found exclusively in the hindgut of the wood-eating cockroach Cryptocercus.We sequenced small subunit ribosomal RNA (SSU rRNA) from total gut DNA to describe Saccinobaculus SSU rRNA diversity. We also sequenced SSU rRNA from manually isolated cells of the two most abundant and readily identifiable species: the type species Saccinobaculus ambloaxostylus and the taxonomically contentious Saccinobaculus doroaxostylus. We inferred phylogenetic trees including all five known oxymonad subgroups in order to elucidate the internal phylogeny of this poorly studied group, to resolve some outstanding issues of the taxonomy and identification of certain Saccinobaculus species, and to investigate the evolution of character states within it. Our analysis recovered strong support for the existence of the five subgroups of oxymonads, and consistently united the subgroups containing Monocercomonoides and Streblomastix, but was unable to resolve any further higher-order branching patterns. & 2006 Elsevier GmbH. All rights reserved. Key words: oxymonad; phylogeny; SSU rRNA; symbiont. Introduction Oxymonads are a group of anaerobic eukaryotic discernable mitochondria and Golgi apparatus flagellates that constitute one of the more poorly (Brugerolle and Lee 2000). In terms of their understood groups of protists, in terms of both evolutionary history, their position on the tree of their overall biology and their evolutionary history. eukaryotes has been varied and disputed (Cava- They are nonetheless of great interest in both lier-Smith 1998; Dacks et al. 2001; Hampl et al. regards. In terms of their basic biology, they 2005; Moriya et al. 1998, 2001; Patterson 1994; possess a number of highly complex structural Simpson 2003). They are now generally regarded characteristics and behaviours, but at the same to be members of the excavate eukaryotes, a time lack typical eukaryotic characters such as diverse collection of flagellates and amoebofla- gellates that includes many parasites and anae- 1 Corresponding author; robes (Simpson 2003). Molecular data support a fax 1 604 822 6089 close relationship between oxymonads and the e-mail [email protected] (P.J. Keeling). excavate flagellate Trimastix (Dacks et al. 2001), & 2006 Elsevier GmbH. All rights reserved. doi:10.1016/j.protis.2006.05.007 ARTICLE IN PRESS 2 A.A. Heiss and P.J. Keeling but there is no definitive evidence for either their cercomonoides globus. Three distinct species higher-order position or their relationship to other were described, S. ambloaxostylus (the type excavate protists (Hampl et al. 2005; Simpson species, and the most abundant), S. doroaxosty- 2003). Many of the unique characteristics of lus (the largest species, which is in addition oxymonads may be explained by their ecology: morphologically and behaviourally distinct from they are obligate symbionts, found only in the gut S. ambloaxostylus), and S. minor, a looser collec- lumen of animals. A few inhabit the guts of tion of small flagellates. Beyond these three vertebrates, but most of the known diversity of species, Cleveland et al. (1934) initially suggested oxymonads is restricted to the hindguts of that as many as six more might exist, but the termites and related xylophagous insects. In the extent of the diversity was difficult to determine at insect environments, oxymonads are members of the time. In subsequent years, subtle details of complex microbial communities. It is likely be- staining properties, observations of granules on or cause of the complexity of these communities that within the axostyle, and studies of reproductive life only one strain, Monocercomonoides strain PA203 histories led to a whittling away of Saccinobaculus (a vertebrate symbiont), has been cultivated diversity as species were reassigned or new (Hampl et al. 2005). This inability to cultivate most groups created. Most significantly, the type oxymonads has meant there are few gene species S. ambloaxostylus was split to create the sequences from any given species, and a general new genus Notila (Cleveland 1950c), S. doroax- lack of molecular data from the group as a whole. ostylus was transferred to Oxymonas as Oxymo- In addition to their uncertain placement nas doroaxostylus (Cleveland 1950a), and the amongst eukaryotes, the lack of molecular data smaller Saccinobaculus species were transferred contributes to a poor understanding of the to Oxymonas as O. nana (Cleveland 1950a). interrelationships among oxymonads. Molecular Here, we provide the first molecular data, small data have been slow in coming, but in recent subunit rRNA (SSU rRNA), from the Saccinobacu- years such data have been obtained for four of the lidae, and by doing so allow the first molecular- five groups of oxymonads (traditionally regarded based analysis of global oxymonad phylogeny. as families): the Pyrsonymphidae (Dacks et al. We combined an environmental-PCR strategy 2001; Moriya et al. 2003), Oxymonadidae (Moriya (sequencing SSU rRNA from the whole gut) to et al. 2003), Streblomastigidae (Keeling and examine overall diversity of the Saccinobaculidae, Leander 2003), and Polymastigidae (Hampl et al. with the manual isolation and characterization of 2005). Resolving the internal phylogeny of this two easily identifiable and key species: the type group will require the molecular characterization of species S. ambloaxostylus and the taxonomically the remaining sub-group, the Saccinobaculidae, ambiguous S. doroaxostylus (O. doroaxostylus). for which there have so far been no molecular data. The members of this last group can be quite Results and Discussion spectacular. They are found in a single natural community within the hindgut of the wood-eating Surveying Phylogenetic Diversity of cockroach Cryptocercus, although in that com- Oxymonads in Cryptocercus by munity they are abundant and diverse. Members Environmental PCR of the family are morphologically so plastic that they defy ready description (Cleveland et al. 1934): We surveyed SSU rRNA sequence diversity from like all oxymonads, they have a prominent the Cryptocercus gut in order to assess the axostyle running along the length of the cell, phylogenetic breadth of oxymonads in this envir- which in the case of Saccinobaculus twists, coils, onment. Amplification with oxymonad-specific writhes, and straightens in a variety of changing primers yielded a single detectable band of patterns within the cell. This movement creates approximately 2100 bp. This fragment was cloned the appearance of a snake (the axostyle) in a bag and sequenced, resulting in 14 unique sequences, (the plasma membrane), from which the name is all most similar to other oxymonad rRNAs. derived (Cleveland et al. 1934). Phylogenetic analysis with the global eukaryotic All members of the Saccinobaculidae were alignment confirmed this by placing all new originally described by Cleveland et al. (1934), sequences within the oxymonad/Trimastix clade who at first classified all of the oxymonads in with 96% support (not shown). Oxymonads C. punctulatus in the genus Saccinobaculus, with generally have larger-than-average SSU rRNA the single exception of the small flagellate Mono- sequences, ranging from about 2000—2900 bp ARTICLE IN PRESS Phylogeny of Saccinobaculus 3 (by contrast, the average eukaryotic sequence is environmental sequences (our Saccinobaculus 1800 bp). The oxymonad genes all have insertions spp. E1—E14) represent an appreciable degree at various points, many of which are shared of sequence diversity, and yet form a single clade amongst the groups of oxymonads (Hampl et al. with 93—100% support to the exclusion of all 2005). other oxymonad groups. Overall, the environmen- We narrowed our focus to oxymonads and tal sequences are all derived from a single Trimastix to allow a greater number of alignable oxymonad lineage, and there is no evidence of sites to be used, a phylogeny of which is shown in close relatives of other sampled oxymonad Figure 1. Here, as in the global analysis, the groups that have been proposed to exist in Saccinobaculus doroaxostylus I 1 Saccinobaculus doroaxostylus E 14 100.0 Saccinobaculus doroaxostylus E 13 100.0 98.1 Saccinobaculus doroaxostylus E 12 96.7 98.1 Saccinobaculus doroaxostylus E 11 97.5 Saccinobaculus sp. E 10 Saccinobaculus sp. E 9 Saccinobaculus ambloaxostylus E 8 Saccinobaculus ambloaxostylus E 6 Saccinobaculus ambloaxostylus E 7 53.6 64.3 Saccinobaculus ambloaxostylus E 5 94.6 Saccinobaculus ambloaxostylus E 4 96.9 Saccinobaculus ambloaxostylus I 2a Saccinobaculus ambloaxostylus I 4b Saccinobaculidae Saccinobaculus ambloaxostylus I 6a Saccinobaculus ambloaxostylus I 6c Saccinobaculus ambloaxostylus I 6b 96.6 Saccinobaculus
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