Evolution of obligate nonnutritional endosymbionts

Obligate nonnutritional endosymbionts come in various guises and graduations Several families of marine fish and squid employ luminous bacteria in displays that are associated with sex-specific signaling, predator avoidance, locating or attracting prey, and schooling The host provides a dedicated organ, the light organ, to host bacteria belonging to the genera Photobacterium and Vibrio (both Vibrionaceae, y-Proteobacteria) . The light organ typically accommodates and nurtures a single light-producing species in an extracellular environment From an immunological point of view, the symbiosis might be considered extracorporeal Accessory tissues control, direct, and diffuse the bacterial light There is species-specificity of the bioluminescent symbiosis in the sense that each fish or squid holds a specific bacterial species or strain This led to proposals of coevolution of host and symbiont that might result in codivergence or cospeciation The host selects the symbiont, which has to be acquired from the environment for each new generation The fact itself that the transmission of the symbionts of fish and squid is horizontal and not vertical should influence the evolutionary outcome of this symbiosis In a terrestrial environment horizontally transmitted symbionts are often limited in their dispersal options, whereas in an aquatic environment dispersal for bacteria is unhindered This might exercise strong selection pressure on terrestrial symbionts In the fish and squid bioluminescent symbiosis, the association is obligate for the fish and squid but not for the symbiotic bacteria The luminous bacteria are not obligately dependent on a host for reproduction; they also can colonize other habitats like intestinal tracts, skin, and body fluids of marine animals, sediment, and even seawater For these symbiotic bacteria no genome reduction should be expected Phylogenetic analyses and reanalyses show that the trees for the fish and squid do not match the trees for the bacteria challenging codivergence in these obligate symbioses (Dunlap et al , 2007)

A strict species specificity of fish/squid and bacteria association would be a dangerous strategy for the host Because the bacteria can reproduce without their hosts, there is limited selection on the bacteria to provide light and the host might end up with a bacte rial species that will yield less and less benefit . Certain squids and fishes have been found with two bacterial species in their light organs (Fidopiastis et al , 1998; Guerrero-Ferreira and Nishiguchi, 2007; Kaeding et al ., 2007) . These are seen as exceptions . We would expect that a host in general would allow low levels of competing bacteria in their symbiotic organs When equal amounts of two species are found, that should indicate that a symbi-ont replacement is in progress

The bioluminescent symbiosis in squid and fish can be regarded as a form of cyclic endosymbiosis, which requires regular reassociation events between symbiotic bacteria and host for every individual in each generation . In a terrestrial environment, cyclic endo-symbiosis can be found, for example, between the fungus Geosiphon pyriforme, which can be found on soil surface, and the intracellular cyanobacterium Nostoc punctiforme (Schufiler et al , 1994) Many facultative and some obligate nutritional insect symbioses are examples of cyclic symbiosis

A terrestrial, obligate, nonnutritional symbiosis has been discovered between a sapro-trophic fungus, Rhizopus microsporus, and an intracellular bacterium belonging to the genus Burkholderia (P-Proteobacteria) (Partida-Martinez et al ., 2007b) . The bacterium provides the fungus with a phytotoxin, rhizoxin A closely related strain of Burkholderia produces in one biotype of the fungus a highly hepatotoxic mycotoxin, rhizonin (Partida-Martinez et al ., 2007a) . The rhizoxin-producing strain of Burkholderia is also essential for the formation of sporangia and spores in the rice seedling blight fungus . Vegetative reproduction is not possible without the endosymbiont The bacterium can still be grown axenically Its large genome size of 3 8 Mbp suggests that it communicates with free-living populations and the association with the fungus is not yet obligate for the endosymbiont Another newly discovered association is between the endosymbiont Cand. Streptomyces philanthi (Acti-nobacteria) in the antennae of 27 species of European beewolf digger wasps (Philanthinae, Hymenoptera) (Kaltenpoth et al ., 2006). The bacterium protects wasp offspring against fungal infections The environmental part of this bacterium is not yet investigated An example for an endosymbiont that has just reached an obligate life style might be Polynu-cleobacter (P-Proteobacteria) in ciliates where it might compensate for a defect in glycoge-nolysis (Vannini et al ., 2007a, 2007b) .

Nonnutritional symbioses where both partners in the association are obligately dependent on each other are formed between nematodes and insects on one side and Wolba-chia pipientis on the other side Wolbachia are transovarially transmitted in nematodes and insects Most filarial nematode species depend on intracellular Wolbachia for embryogenesis and larval development Recently, Wolbachia was also identified in nonfilarial nema-todes (Tsai et al , 2007) The genome sequencing of several Wolbachia strains has not yet revealed any clues about the host-symbiont interactions in filarial nematodes but a nutritional contribution seems unlikely (Heider et al ., 2006) . The parasitoid wasp Asobara tabidia harbors three different strains of Wolbachia All wasp species are haplodiploid Wolbachia induces thelytokous parthenogenesis in many species . One of the strains of Wolbachia in Asobara is essential for oogenesis This strain suppresses apoptosis in nurse cells Nurse cells normally undergo apoptosis during egg development The hypothesis is that the host evolved to compensate for the endosymbiont-induced suppression When the endosym-biont is removed, the host compensation might actually prevent oogenesis (Pannebakker et al , 2007) Thus parasitic inhibition of cell death would facilitate symbiosis (Aanen and Hoekstra, 2007) If Asobara wasps are cured of the final Wolbachia, extensive apoptosis of the nurse cells of mid-stage egg chambers sets in In Wolbachia-infected wasps no apoptosis is observed What is the effect of removing Wolbachia on the egg cell? Wolbachia is obligate for oogenesis in this species If oogenesis stops in a mid-stage egg chamber because oogen-

esis stops, wouldn't the failure of oocyte development at this very stage have apoptosis as a consequence? We would like to propose that apoptosis is a consequence of failing oogenesis and is not related to host compensation . We consider this a more parsimonious explanation . Wolbachia in this case do not inhibit cell death and do not facilitate symbiosis . However, in individuals of this wasp species we see simultaneously Wolbachia strains that are reproductive parasites or pathogenic endosymbionts that might cause parthenogenesis, and that are obligate endosymbionts for oogenesis, strongly suggesting that obligate relationships evolve from pathogenic or parasitic associations . A mutant Drosophila melanogaster strain has also become dependent on Wolbachia for oogenesis Wolbachia restores oogenesis in mutant females prevented from making eggs by protein-coding lesions in Sex-lethal (Sxl), the master regulator of sex determination (Starr and Cline, 2002) . An overlap of two phenotypes is seen in adzuki bean borer moth, Ostrinia scapulalis, and a sister species, O. furnacalis . In a Wolbachia-infected strain, males selectively die during larval development, whereas females selectively die when Wolbachia are eliminated by antibiotic treatment (Sakamoto et al ., 2007) . Death in the female line occurred mainly throughout early larval stages but development to the penultimate instar was possible Wolbachia is here both a male killer and a sex-specific obligate endosymbiont. Females are heterogametic in moths . In the black twig borer or ambrosia beetle, Xyleborus ferrugineus (Curculionidae, Coleoptera), a morphologically identified Staphylococcus endosymbiont and a nonidentified rod-shaped bacterium are essential for egg development (Peleg and Norris, 1972, 1973; Norris and Chu, 1980). The symbiont(s) is/are intracellular and transovarially transmitted . The beetle is haplodiploid and reproduces through arrhenotokous parthenogenesis . The date stone beetle, Coccotrypes dactyliperda (Curculionidae, Coleoptera), suffers a similar breakdown of oogenesis when treated with antibiotics (Zchori-Fein et al ., 2006). It is also hap-lodiploid and reproduces through arrhenotokous parthenogenesis The date stone beetles carry a double infection of a Wolbachia strain and a Rickettsia strain . Both are transovarially transmitted . Antibiotic treatment affects Wolbachia and Rickettsia equally. One of the two or both are obligate endosymbionts Is one of them trying to replace the other?

Rickettsia have been found in parthenogenetic species of the barklouse, Cerobasis guest-falica, and the booklouse, Liposcelis bostrychophila (Perotti et al , 2006) Two populations of C. guestfalica from Wales, one from the Island of Anglesey (Ynys Mon) and one from the mainland, tested positive. Three populations of L. bostrychophila, one each from England, Wales, and the Czech Republic, were positive . All individuals tested of a population sample harbored Rickettsia . Rickettsial sequences were also reported for three populations in China (Wang et al , 2006) The Rickettsia in L. bostrychophila are transovarially transmitted Removal of the bacteria stops oogenesis The same is assumed for C. guestfalica as well but the proof is still outstanding because of difficulties of putting this species in culture C. guestfalica belongs to the family Trogiidae in the suborder Trogiomorpha, which forms a basal or primitive lineage in the booklice and barklice order Psocoptera . Rickettsia-like organisms have also been detected previously in another family of this suborder Bacteria have been found in the ovaries, eggs, and Malpighian tubules of the barklouse Dorypteryx pallida (Psyllipsocidea) (Hertig and Wolbach, 1924). The presence of bacteria in the eggs shows transovarial transmission However, Rickettsia cannot morphologically be differentiated from Wolbachia. L. bostrychophila, on the other hand, is part of the family Liposceli-dae, which is considered one of the most derived lineages and is phylogenetically closer to the members of the biting and chewing lice order Phthiraptera than to the other psocids The Rickettsia in the two psocid lineages are evolutionary as far apart from each other as the hosts are (Figure 10 1) Indeed, the basal Cerobasis hosts a Rickettsia that associates with equal basal Rickettsia isolates from crane flies, leeches, and amoeba . The closest sequenced relative to the barklouse Rickettsia is currently R. limoniae from crane flies . The Liposcelis Rickettsia form a group with R. felis and the bacterium found in a parthenogenetic wasp species (Figure 10 2) These Rickettsia form a sister group to R. australis and R. akari, which are transmitted by ticks and mites

The Rickettsia in the date stone beetle and the two psocid lineages should not be isolated occurrences Several sexually reproducing psocid species have tested negative for Rickettsia. We should expect to find Rickettsia in related, sexual species . In these species, we would like to predict that the Rickettsia still express low levels of pathogenicity to their hosts . In Wolbachia and Orientia we have seen large numbers of ankyrins-repeat genes most likely involved in host manipulation Should we expect an increased number of ankyrins-repeat genes also in the oogenesis manipulating, obligate Rickettsia?

The obligate psocid Rickettsia exhibit several phenotypic behaviors that can be interpreted as transitional stages in their evolution of host-parasite interaction (Perotti et al ., 2006) Rickettsia enter the developing oocyte both through the germ line and through the nurse cells . Germ line transmission is characteristic for reproductive parasites like Wolba-chia, whereas nutritional endosymbionts often reach the oocytes through nurse cells In a few of the psocids examined, one of the paired mycetomes was duplicated (Figure 10 . 2) and additional Malpighian tubules appeared Organ duplication is very rare during the development of insects The duplication of these organs could indicate a still ongoing process in the host of fine-tuning recently evolved provisions for obligate endosymbionts Primary endosymbionts only reside in mycetomes in well-established systems of nutritional symbiosis Psocid Rickettsia are found not only in mycetomes but also in many other tissues

In the obligate systems described for the beetle and booklice, the association is obligatory for both partners The Rickettsia in the booklice can no longer leave their host We would predict that the genomes of these Rickettsia strains should show further genome reduction than the human pathogenic Rickettsia sequenced so far.

Genome reduction and genome isolation are linked There is only one possible evolutionary outcome, degradation . Because of genome reduction and isolation, obligate endo-symbionts will have a finite lifespan as a species or a limited shelf life as a functional endosymbiont The provision of the symbiont to the host will eventually degrade to a point were it might severely affect the host In order not to go under with its symbiont, the host must allow for the eventual replacement of the symbiont This means that the host must allow limited concurrent infections with slightly pathogenic bacteria A bacterium has to be infectious to invade a new host species . The bacterium will be naive to the new host and involuntarily cause some pathology The new bacteria have to infect the host intracellularly to escape the immune system

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