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Exclusive Gut Flagellates of Serritermitidae Suggest a Major Transfaunation Event in Lower Termites: Description of Heliconympha glossotermitis gen. nov. spec. nov

DOI:10.1111/jeu.12441
Authors:
Renate Radek at Freie Universität Berlin
Renate Radek
Katja Meuser at Max Planck Institute for Terrestrial Microbiology
Katja Meuser
Jürgen F. H. Strassert
Jürgen F. H. Strassert
Jürgen F. H. Strassert
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Oguzhan Arslan
Oguzhan Arslan
Oguzhan Arslan
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Abstract

The guts of lower termites are inhabited by host-specific consortia of cellulose-digesting flagellate protists. In this first investigation of the symbionts of the family Serritermitidae, we found that Glossotermes oculatus and Serritermes serrifer each harbor similar parabasalid morphotypes: large Pseudotrichonympha-like cells, medium-sized Leptospironympha-like cells with spiraled bands of flagella, and small Hexamastix-like cells; oxymonadid flagellates were absent. Despite their morphological resemblance to Pseudotrichonympha and Leptospironympha, a SSU rRNA-based phylogenetic analysis identified the two larger, trichonymphid flagellates as deep-branching sister groups of Teranymphidae, with Leptospironympha sp. (the only spirotrichosomid with sequence data) in a moderately supported basal position. Only the Hexamastix-like flagellates are closely related to trichomonadid flagellates from Rhinotermitidae. The presence of two deep-branching lineages of trichonymphid flagellates in Serritermitidae and the absence of all taxa characteristic of the ancestral rhinotermitids underscores that the flagellate assemblages in the hindguts of lower termites were shaped not only by a progressive loss of flagellates during vertical inheritance but also by occasional transfaunation events, where flagellates were transferred horizontally between members of different termite families. In addition to the molecular phylogenetic analyses, we present a detailed morphological characterization of the new spirotrichosomid genus Heliconympha using light and electron microscopy. This article is protected by copyright. All rights reserved.
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Max-Planck-Institut • Karl-von-Frisch-Strasse 10 • 35043 Marburg • Germany Prof. Dr. Andreas Brune
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... Initial investigations on these symbioses suggested that termite-protist associations are rather specific and evolutionarily stable (Kitade, 2004). Recent phylogenetic analyses indicated that the evolutionary codiversification between lower termites and their gut protists is mostly characterized by cospeciation, although occasional events of host switching and symbiont loss were also evidenced (Desai et al., 2010;Noda et al., 2007;Radek et al., 2018;Taerum, De Martini, Liebig, & Gile, 2018). ...
... As in many other mutualistic symbioses where hosts and symbionts are mutually dependent for survival and reproduction (Moran, McCutcheon, & Nakabachi, 2008;Salem et al., 2015), it is generally assumed that co-speciation between gut protists and lower termites emerged as a direct consequence of an efficient vertical transmission of protists across termite generations (Desai et al., 2010;Noda et al., 2007;Radek et al., 2018;Taerum et al., 2018). The results of the present study constitute the first empirical evidence supporting this widely held assumption. ...
... We propose two nonexclusive hypothetical mechanisms that could provide preliminary answers to this question. First, recent phylogenetic analyses have revealed that protists can occasionally be transferred horizontally between termite species (Desai et al., 2010;Noda et al., 2007;Radek et al., 2018;Taerum et al., 2018). We cannot exclude that such horizontal transmission events also occurred within termite species. ...
Efficient but occasionally imperfect vertical transmission of gut mutualistic protists in a wood‐feeding termite
Article
Full-text available
  • Jan 2020
Although mutualistic associations between animals and microbial symbionts are widespread in nature, the mechanisms that have promoted their evolutionary persistence remain poorly understood. A vertical mode of symbiont transmission (from parents to offspring) is thought to ensure partner fidelity and stabilisation, although the efficiency of vertical transmission has rarely been investigated, especially in cases where hosts harbour a diverse microbial community. Here we evaluated vertical transmission rates of cellulolytic gut oxymonad and parabasalid protists in the wood‐feeding termite Reticulitermes grassei. We sequenced amplicons of the 18S rRNA gene of protists from 24 colonies of R. grassei collected in two populations. For each colony, the protist community was characterised from the gut of 14 swarming reproductives and from a pool of 10 worker guts. A total of 98 OTUs belonging to 13 species‐level taxa were found. The vertical transmission rate was estimated for each protist present in a colony by its frequency among the reproductives. Results revealed that transmission rates were high, with an average of 0.897 (±0.164) per protist species. Overall, the protist community did not differ between reproductive sexes, suggesting that both the queen and king could contribute to the gut microbiota of the offspring. A positive relationship between the transmission rate of protists and their prevalence within populations was also detected. However, transmission rates alone did not explain protist prevalence. In conclusion, these findings reveal key forces behind a conserved, multi‐species mutualism, raising further questions on the roles of horizontal transfer and negative selection in shaping symbiont prevalence.
... The cellulolytic protists found in the guts of all "lower" termites and Cryptocercus originate from two independent groups, Parabasalia and Oxymonadida (Preaxostyla) [17,18]. Gut protists have evolved through varying degrees of horizontal transfer and episodes of co-speciation with their hosts [18][19][20][21][22][23][24]. In some species of Cryptocercus, there can be up to 25 species of protists. ...
... By contrast, many termite species host a limited number of protist species. This is especially true for more phylogenetically derived species of termites [23], such as certain Rhinotermitidae that are associated with a handful of protist species, down to a single species in Termitogeton [25]. This reduction in symbiont diversity portends the complete loss of protists in one termite lineage nested within the paraphyletic Rhinotermitidae-the Termitidae (i.e., "higher" termites: Fig. 1). ...
... However, we here support the hypothesis that two distinct mutualistic shifts had a critical role within the history of termite evolution: (1) the initial acquisition of intestinal protists within the context of alloparental care as one of the key events that enabled or facilitated the emergence of eusociality in termites, and (2) the much later loss of these protists, associated with the gain of alternative mutualists, that ultimately triggered the emergence of the most successful termite group, the Termitidae. Interestingly, there is a progressive loss of protozoan diversity in more derived "lower" termites [23,25], which culminates in their complete loss in the "higher" termites. Regardless of the factors that led to this protistan disappearance from the guts, they presumably cascaded a series of changes that fundamentally altered the inherent physiology and ecological performance of Termitidae. ...
Termite evolution: mutualistic associations, key innovations, and the rise of Termitidae
Article
Full-text available
Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all “lower” termites rely on cellulolytic protists to digest wood, “higher” termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by “lower” termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of “higher” termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.
... More recently, ultrastructural studies demonstrated that the flagella of Microjoenia arise from very short, longitudinal to slightly spiraling bands, confirming its Spirotrichonymphea affinities (Brugerolle 2001). Note that while Spirotrichosomidae (Trichonymphida, Parabasalia) also feature spiraling rows of flagella, they emerge from bilaterally symmetrical rostral structures characteristic of Trichonymphida, and their flagellar bands form a lefthanded helix (Carpenter et al. 2010;Radek et al. 2018), thus excluding Microjoenia. The simple, tubular axostyle links Microjoenia specifically with Spironympha (Brugerolle 2005; Brugerolle and Bordereau 2006), another genus that currently lacks molecular data. ...
Molecular Phylogenetic Position of Microjoenia (Parabasalia: Spirotrichonymphea) from Reticulitermes and Hodotermopsis Termite Hosts
Article
Microjoenia are obligate symbionts of termites. The genus was erected in 1892 for small cells with many flagella that insert near, but not directly from, the cell apex, and an axostyle that can protrude from the cell posterior. Although ultrastructural studies have been carried out on three Microjoenia species to date, no molecular data have been directly attributed to any species. Microjoenia are classified within the parabasalian class Spirotrichonymphea, which is characterized by flagellar bands that emerge near the cell apex and proceed posteriorly in a right-handed helix. In Microjoenia, however, the flagellar bands are very short and proceed longitudinally or with a weakly observable helix. In this study, we have amplified and sequenced the 18S ribosomal RNA gene from individually isolated Microjoenia cells from Reticulitermes and Hodotermopsis hosts as part of an ongoing effort to understand the phylogeny of Spirotrichonymphea and their coevolution with termites. In our 18S rRNA gene phylogeny, Microjoenia forms the sister lineage to Spirotrichonympha, though many other evolutionary relationships within Spirotrichonymphea remain unresolved.
... This would explain the distinct protist community found in Reticulitermes as compared to its rhinotermitid relatives (Kitade, 2004). Another ancient HST may have occurred in the ancestor of Serritermes and Glossotermes (Serritermitidae), again explaining why the symbionts of these host genera differ from those of their rhinotermitid relatives (Radek et al., 2018). To date these are the only two documented inferences of HST in termites. ...
Biogeography and Independent Diversification in the Protist Symbiont Community of Heterotermes tenuis
Article
Full-text available
  • Mar 2021
The eukaryotic microbiome of “lower” termites is highly stable and host-specific. This is due to the mutually obligate nature of the symbiosis and the direct inheritance of protists by proctodeal trophallaxis. However, vertical transmission is occasionally imperfect, resulting in daughter colonies that lack one or more of the expected protist species. This phenomenon could conceivably lead to regional differences in protist community composition within a host species. Here, we have characterized the protist symbiont community of Heterotermes tenuis (Hagen) (Blattodea: Rhinotermitidae) from samples spanning South and Central America. Using light microscopy, single cell isolation, and amplicon sequencing, we report eight species-level protist phylotypes belonging to four genera in the phylum Parabasalia. The diversity and distribution of each phylotype’s 18S rRNA amplicon sequence variants (ASVs) mostly did not correlate with geographical or host genetic distances according to Mantel tests, consistent with the lack of correlation we observed between host genetic and geographical distances. However, the ASV distances of Holomastigotoides Ht3 were significantly correlated with geography while those of Holomastigotoides Ht1 were significantly correlated with host phylogeny. These results suggest mechanisms by which termite-associated protist species may diversify independently of each other and of their hosts, shedding light on the coevolutionary dynamics of this important symbiosis.
... They also share a largely similar and unusual linear development combined with the presence of all-male pseudergates (Bourguignon et al. 2009;Barbosa and Constantino 2017). Finally, their gut protist consortia are highly similar and unique among "lower" termites (Radek et al. 2018). ...
The trail-following pheromone of the termite Serritermes serrifer
Article
Full-text available
The Neotropical family Serritermitidae is a monophyletic group of termites including two genera, Serritermes and Glossotermes, with different way-of-life, the former being the sole obligatory inquiline among “lower” termites, while the latter is a single-site nester feeding on dry rotten red wood. Like the most advanced termite’s family, the Termitidae, the Serritermitidae is an inner group of the paraphyletic family “Rhinotermitidae”, but unlike the Termitidae, it has been poorly studied so far. In this study, we bring new insights into the chemical ecology of this key taxon. We studied the trail-following pheromone of Serritermes serrifer and we identified (10Z,13Z)-nonadeca-10,13-dien-2-one as the only component of the trail-following pheromone of this termite species, as it is the case in Glossotermes, the other genus belonging to Serritermitidae. This result makes the family Serritermitidae clearly distinct from other Rhinotermitidae, such as the termites Psammotermes and Prorhinotermes, that use (3Z,6Z,8E)-dodeca-3,6,8-trien-1-ol and/or neocembrene as trail-following pheromones.
... Vertical transmission has led to co-speciation between bacteria and their protist hosts, and sometimes even the termite hosts [26][27][28][29]. Evidence for horizontal transfer of protists between termite species, so called transfaunations, is limited to a few exceptions [30]. Hence, the termite host species association is rather strict, leading to strong phylogenetic imprints on protist community structure [31][32][33]. ...
Ecological specificity of the metagenome in a set of lower termite species supports contribution of the microbiome to adaptation of the host
Article
Full-text available
  • Oct 2019
Background Elucidating the interplay between hosts and their microbiomes in ecological adaptation has become a central theme in evolutionary biology. A textbook example of microbiome-mediated adaptation is the adaptation of lower termites to a wood-based diet, as they depend on their gut microbiome to digest wood. Lower termites have further adapted to different life types. Termites of the wood-dwelling life type never leave their nests and feed on a uniform diet. Termites of the foraging life type forage for food outside the nest and have access to other nutrients. Here we sought to investigate whether the microbiome that is involved in food substrate breakdown and nutrient acquisition might contribute to adaptation to these dietary differences. We reasoned that this should leave ecological imprints on the microbiome. Results We investigated the protist and bacterial microbiomes of a total of 29 replicate colonies from five termite species, covering both life types, using metagenomic shotgun sequencing. The microbiome of wood-dwelling species with a uniform wood diet was enriched for genes involved in lignocellulose degradation. Furthermore, metagenomic patterns suggest that the microbiome of wood-dwelling species relied primarily on direct fixation of atmospheric nitrogen, while the microbiome of foraging species entailed the necessary pathways to utilize nitrogen in the form of nitrate for example from soil. Conclusion Our findings are consistent with the notion that the microbiome of wood-dwelling species bears an imprint of its specialization on degrading a uniform wood diet, while the microbiome of the foraging species might reflect its adaption to access growth limiting nutrients from more diverse sources. This supports the idea that specific subsets of functions encoded by the microbiome can contribute to host adaptation.
Phylogenetic Identification of Symbiotic Protists of Five Chinese Reticulitermes Species Indicates a Cospeciation of Gut Microfauna with Host Termites
Article
  • Jun 2021
Symbiotic protists play important roles in the wood digestion of lower termites. Previous studies showed that termites generally possess host‐specific flagellate communities. The genus Reticulitermes is particularly interesting because its unique assemblage of gut flagellates bears evidence for transfaunation. The gut fauna of Reticulitermes species in Japan, Europe, and North America had been investigated, but data on species in China is scarce. For the first time we analyzed the phylogeny of protists in the hindgut of five Reticulitermes species in China. A total of 22 protist phylotypes were affiliated with the family Trichonymphidae, Teranymphidae, Trichomonadidae and Holomastigotoididae (Phylum Parabasalia), and 45 protist phylotypes were affiliated with the family Pyrsonymphidae (Phylum Preaxostyla). The protist fauna of these five Reticulitermes species is similar to those of Reticulitermes species in the other geographical regions. The topology of Trichonymphidae subtree was similar to that of Reticulitermes tree. All Preaxostyla clones were affiliated with the genera Pyrsonympha and Dinenympha (Order Oxymonadida) as in the other Reticulitermes species. The results of this study not only add to the existing information on the flagellates present in other Reticulitermes species but also offer the opportunity to test the hypotheses for the coevolution of symbiotic protists with their host termites.
The Complete Protist Symbiont Communities of Coptotermes formosanus and Coptotermes gestroi : Morphological and Molecular Characterization of Five New Species
Article
  • Jun 2020
Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann) (Blattoidea: Rhinotermitidae) are invasive subterranean termite pest species with a major global economic impact. However, the descriptions of the mutualistic protist communities harbored in their respective hindguts remain fragmentary. The C. formosanus hindgut has long been considered to harbor three protist species, Pseudotrichonympha grassii (Trichonymphida), Holomastigotoides hartmanni , and Cononympha (Spirotrichonympha ) leidyi (Spirotrichonymphida), but molecular data have suggested that the diversity may be higher. Meanwhile, the C. gestroi community remains undescribed except for Pseudotrichonympha leei . To complete the characterization of these communities, hindguts of workers from both termite species were investigated using single cell PCR, microscopy, cell counts, and 18S rRNA amplicon sequencing. The two hosts were found to harbor intriguingly parallel protist communities, each consisting of one Pseudotrichonympha species, two Holomastigotoides species, and two Cononympha species. All protist species were unique to their respective hosts, which last shared a common ancestor ~ 18 MYA. The relative abundances of protist species in each hindgut differed remarkably between cell count data and 18S rRNA profiles, calling for caution in interpreting species abundances from amplicon data. This study will enable future research in C. formosanus and C. gestroi hybrids, which provide a unique opportunity to study protist community inheritance, compatibility, and potential contribution to hybrid vigor.
Novel Lineages of Oxymonad Flagellates from the Termite Porotermes adamsoni (Stolotermitidae): the Genera Oxynympha and Termitimonas
Article
The symbiotic gut flagellates of lower termites form host-specific consortia composed of Parabasalia and Oxymonadida. The analysis of their coevolution with termites is hampered by a lack of information, particularly on the flagellates colonizing the basal host lineages. To date, there are no reports on the presence of oxymonads in termites of the family Stolotermitidae. We discovered three novel, deep-branching lineages of oxymonads in a member of this family, the damp-wood termite Porotermes adamsoni. One tiny species (6-10μm), Termitimonas travisi, morphologically resembles members of the genus Monocercomonoides, but its SSU rRNA genes are highly dissimilar to recently published sequences of Polymastigidae from cockroaches and vertebrates. A second small species (9-13μm), Oxynympha loricata, has a slight phylogenetic affinity to members of the Saccinobaculidae, which are found exclusively in wood-feeding cockroaches of the genus Cryptocercus, the closest relatives of termites, but shows a combination of morphological features that is unprecedented in any oxymonad family. The third, very rare species is larger and possesses a contractile axostyle; it represents a phylogenetic sister group to the Oxymonadidae. These findings significantly advance our understanding of the diversity of oxymonads in termite guts and the evolutionary history of symbiotic digestion.
Molecular phylogenetic position of Hoplonympha natator (Trichonymphea, Parabasalia)
Article
  • Sep 2019
Hoplonympha natator is an obligate symbiont of Paraneotermes simplicicornis (Kalotermitidae), from southwestern North America. Another Hoplonympha species inhabits Hodotermopsis sjostedti (Archotermopsidae), from montane Southeast Asia. The large phylogenetic and geographical distance between the hosts makes the distribution of Hoplonympha puzzling. Here we report the phylogenetic position of H. natator from P. simplicicornis through maximum likelihood and Bayesian analysis of 18S rRNA genes. The two Hoplonympha species form a clade with a deep node, making a recent symbiont transfer unlikely. The distribution of Hoplonympha may be due to an ancient transfer or strict vertical inheritance with differential loss from other hosts.
Polymorphism in the neotropical termite Serritermes serrifer
Article
Serritermitidae (Isoptera) is a small and little known Neotropical termite family which includes only two genera: Glossotermes and Serritermes. Despite the lack of detailed studies, it has been assumed that these termites have a true worker caste. A recent study revealed that Glossotermes has a linear development pathway and lacks true workers. Here, we present a study of the polymorphism of Serritermes serrifer Hagen & Bates, a species endemic to the Cerrado ecoregion of central Brazil which lives as an inquiline inside nests of Cornitermes spp. A morphometric analysis was performed based on measurements taken of 11 body parts of 544 specimens of immatures, worker-like individuals, soldiers, and alates. Sex of specimens was determined by dissection and examination of the seventh sternite. A principal component analysis (PCA) was used to evaluate morphological changes during development. Contrary with previous information from the literature and similar to Glossotermes, Serritermes shows a linear development pathway with two larval instars, two sizes of pseudergates, and a single nymphal morph. Pseudergates apparently undergo stationary molts. Sex ratio among pseudergates is male-biased, but not as strongly as in Glossotermes. Typical colonies have a single physogastric primary queen and a single primary king. Ergatoid reproductives are relatively rare and some female ergatoids may become strongly physogastric. Nymphoid reproductives were not found. All soldiers are male and bear well-developed testes.
Systematic differentiation and evolution of flagellates in termites
Article
Flagellates of the Orders Trichomonadida Kirby, Oxymonadida Grasse, and Hypermastigida Grassi and Foa Reported from Lower Termites (Isoptera Families Mastotermitidae, Kalotermitidae, Hodotermitidae, Termopsidae, Rhinotermitidae, and Serritermitidae) and from the Wood-Feeding Roach Cryptocercus (Dictyoptera, Cryptocercidae)
Article
Frontal gland dehiscence in the Brazilian termite Serritermes serrifer (Isoptera: Serritermitidae)
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Spirotrichonymphidae of Stolotermes
Article
  • Jan 1958
Characteristics of the symbiotic flagellate composition within the termite family Rhinotermitidae (Isoptera)
Article
All lower termites contain a symbiotic flagellate community in their hindguts. Yamin (1979) listed the symbiotic protistan composition of 31 species that belong to the family Rhinotermitidae. In this study, the symbiont composition of additional 23 Rhinotermitid termite species were investigated. The flagellate genera Spirotrichonympha, Pseudotrichonympha and Holomastigotoides are prevalent among Rhinotermitid hosts. Members of the genus Reticulitermes lack the latter two flagellate genera, but possess the most diverse flagellate community of the Rhinotermitids, being the only genus to contain flagellates of the order Oxymonadida. A one to one host-species to symbiont-species relationship is found within the genera Parrhinotermes and Termitogeton.
Establishment of symbiotic flagellate fauna of Hodotermopsis japonica (Isoptera: Termopsidae)
Article
The process of symbiotic flagellate infection of newly hatched larvae was investigated on a damp wood termite Hodotermopsis japonica. Transmission of flagellate species begins from the 1st instar larvae 1-2 days after hatching. The complete fauna is established in a majority of 2nd instar larvae, and all of the 3rd instar larvae examined have the complete fauna. The time to establish the symbiont fauna is quicker than that of Reticulitermes speratus.
Experimental transfaunation of termites
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The termite family Serritermitidae (Isoptera)
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Morphology and evolution of intestinal parasitic flagellates of the Far Eastern roach Cryptocercus relictus
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  • Jan 1975