Arsenophonus

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Arsenophonus
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Bacteria
Phylum: Pseudomonadota
Class: Gammaproteobacteria
Order: Enterobacterales
Family: Morganellaceae
Genus: Arsenophonus
Gherna et al. 1991
Type species
Arsenophonus nasoniae [1]
Species [1]

Arsenophonus is a genus of Morganellaceae, of the Gammaproteobacteria. [2] Members of the Arsenophonus genus are increasingly discovered bacterial symbionts of arthropods that are estimated to infect over 5% of arthropod species globally [3] and form a variety of relationships with hosts across the mutualism parasitism continuum. Arsenophonus bacteria have been identified in a diversity of insect taxa, including economically important species such as the Western honey bee [4] [5] and the rice pest Nilaparvata lugens . [6]

Contents

The majority of work on Arsenophonus has been done on the type species Arsenophonus nasoniae for which genetic manipulation has been successful in achieving in vivo tracking of the bacterium. [7] Arsenophonus nasoniae infects Nasonia parasitic wasps, [8] [1] is vertically transmitted, passed from a female wasp to the fly host during parasitisation, and then acquired by her hatching larvae feeding on the microbe [9] . It has a male-killing phenotype. Infection with Arsenophonus nasoniae triggers the death of approximately 80% of the wasps male offspring. [10] [11] Killing male offspring is thought to facilitate the spread of Arsenophonus through the host population as it releases more resources to female offspring, and it is the female line that Arsenophonus is transmitted through. [12] [13] . However, horizontal transmission during superparasitism of a single fly pupae by multiple wasp females is required for symbiont spread [14] .

Within the genus a number of Arsenophonus strains have known roles as mutualistic endosymbionts. [15] In both Pediculus humanus [16] and Lipoptena cervi [17] Arsenophonus symbionts are essential to host functioning and are involved in vitamin synthesis, and are vertically transmitted across host generations. In other hosts Arsenophonus is suspected to be parasitic. In the Western honey bee Arsenophonus can be horizontally transmitted via social behaviour, [5] and the presence of Arsenophonus in a colony has been linked to poor bee health. [18] [19] This species has been formally described as Arsenophonus apicola. [20] The majority of associations between Arsenophonus and host taxa remain uncharacterized.

The diversity of interactions between Arsenophonus and insects has led to the genus being adopted, alongside Sodalis , as one where it is possible to investigate the genetic and evolutionary changes associated with different types of symbiosis. Siozios et al [21] demonstrated early stages of transition to vertical (parent-offspring) transmission were associated with increases in Arsenophonus genome size, associated with proliferation of prophage. This was considered a consequence of loss of CRISPR-Cas defences, hypothesized to be driven by reduce phage predation rates in strongly host associated endosymbionts. Indeed, Arsenophonus nasoniae has one of the more complex microbial genomes, carrying over 50 prophage elements and 17 plasmids [22] .

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<span class="mw-page-title-main">Endosymbiont</span> Organism that lives within the body or cells of another organism

An endosymbiont or endobiont is an organism that lives within the body or cells of another organism. Typically the two organisms are in a mutualistic relationship. Examples are nitrogen-fixing bacteria, which live in the root nodules of legumes, single-cell algae inside reef-building corals, and bacterial endosymbionts that provide essential nutrients to insects.

<i>Wolbachia</i> Genus of bacteria in the Alphaproteobacteria class

Wolbachia is a genus of gram-negative bacteria infecting many species of arthropods and filarial nematodes. The symbiotic relationship ranges from parasitism to obligate mutualism. It is one of the most common parasitic microbes of arthropods, and is possibly the most widespread reproductive parasite bacterium in the biosphere. Its interactions with hosts are complex and highly diverse across different host species. Some host species cannot reproduce, or even survive, without Wolbachia colonisation. One study concluded that more than 16% of neotropical insect species carry bacteria of this genus, and as many as 25 to 70% of all insect species are estimated to be potential hosts.

<i>Spiroplasma</i> Genus of bacteria

Spiroplasma is a genus of Mollicutes, a group of small bacteria without cell walls. Spiroplasma shares the simple metabolism, parasitic lifestyle, fried-egg colony morphology and small genome of other Mollicutes, but has a distinctive helical morphology, unlike Mycoplasma. It has a spiral shape and moves in a corkscrew motion. Many Spiroplasma are found either in the gut or haemolymph of insects where they can act to manipulate host reproduction, or defend the host as endosymbionts. Spiroplasma are also disease-causing agents in the phloem of plants. Spiroplasmas are fastidious organisms, which require a rich culture medium. Typically they grow well at 30 °C, but not at 37 °C. A few species, notably Spiroplasma mirum, grow well at 37 °C, and cause cataracts and neurological damage in suckling mice. The best studied species of spiroplasmas are Spiroplasma poulsonii, a reproductive manipulator and defensive insect symbiont, Spiroplasma citri, the causative agent of citrus stubborn disease, and Spiroplasma kunkelii, the causative agent of corn stunt disease.

<span class="mw-page-title-main">Genome size</span> Amount of DNA contained in a genome

Genome size is the total amount of DNA contained within one copy of a single complete genome. It is typically measured in terms of mass in picograms or less frequently in daltons, or as the total number of nucleotide base pairs, usually in megabases. One picogram is equal to 978 megabases. In diploid organisms, genome size is often used interchangeably with the term C-value.

<i>Buchnera aphidicola</i> Species of bacterium

Buchnera aphidicola, a member of the Pseudomonadota and the only species in the genus Buchnera, is the primary endosymbiont of aphids, and has been studied in the pea aphid, Acyrthosiphon pisum. Buchnera is believed to have had a free-living, Gram-negative ancestor similar to a modern Enterobacterales, such as Escherichia coli. Buchnera is 3 μm in diameter and has some of the key characteristics of its Enterobacterales relatives, such as a Gram-negative cell wall. However, unlike most other Gram-negative bacteria, Buchnera lacks the genes to produce lipopolysaccharides for its outer membrane. The long association with aphids and the limitation of crossover events due to strictly vertical transmission has seen the deletion of genes required for anaerobic respiration, the synthesis of amino sugars, fatty acids, phospholipids, and complex carbohydrates. This has resulted not only in one of the smallest known genomes of any living organism, but also one of the most genetically stable.

<i>Nasonia</i> Genus of wasps

Nasonia are a genus of small pteromalid parasitoid wasps that sting and lay eggs in the pupae of various flies. The fly species that Nasonia usually parasitize are primarily blow flies and flesh flies, making Nasonia a useful tool for biocontrol of these pest flies. The small match-head sized wasps are also referred to as jewel wasps based on the emerald sheen of their exoskeleton.

<i>Nasonia vitripennis</i> Species of insect

Nasonia vitripennis is one of four known species under the genus Nasonia - small parasitoid wasps that afflict the larvae of parasitic carrion flies such as blowflies and flesh flies, which themselves are parasitic toward nestling birds. It is the best known and most widely studied of the parasitoid wasps, and their study forms a vital part of the information used to describe the order Hymenoptera, along with information from bees and ants. This parasitoid behaviour makes the wasps an interest for the development of biopesticide and biological systems for controlling unwanted insects.

Blattabacterium is a genus of obligate mutualistic endosymbiont bacteria that are believed to inhabit all species of cockroach studied to date, with the exception of the genus Nocticola. The genus' presence in the termite Mastotermes darwiniensis led to speculation, later confirmed, that termites and cockroaches are evolutionarily linked.

Cytoplasmic incompatibility (CI) is a mating incompatibility reported in many arthropod species that is caused by intracellular parasites such as Wolbachia. These bacteria reside in the cytoplasm of the host cells and modify their hosts' sperm in a way that leads to embryo death unless this modification is 'rescued' by the same bacteria in the eggs. CI has been reported in many insect species, as well as in mites and woodlice. Aside from Wolbachia, CI can be induced by the bacteria Cardinium,Rickettsiella, Candidatus Mesenet longicola and Spiroplasma. CI is currently being exploited as a mechanism for Wolbachia-mediated disease control in mosquitoes.

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Serratia symbiotica is a species of bacteria that lives as a symbiont of aphids. In the aphid Cinara cedri, it coexists with Buchnera aphidicola, given the latter cannot produce tryptophan. It is also known to habitate in Aphis fabae. Together with other endosymbionts, it provides aphids protection against parasitoids.

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Arsenophonus nasoniae is a species of bacterium which was previously isolated from Nasonia vitripennis, a species of parasitoid wasp. These wasps are generalists which afflict the larvae of parasitic carrion flies such as blowflies, houseflies and flesh flies. A. nasoniae belongs to the phylum Pseudomonadota and family Morganellaceae. The genus Arsenophonus, has a close relationship to the Proteus (bacterium) rather than to that of Salmonella and Escherichia. The genus is composed of gammaproteobacterial, secondary-endosymbionts which are gram-negative. Cells are non-flagellated, non-motile, non-spore forming and form long to highly filamentous rods. Cellular division is exhibited through septation. The name 'Arsenophonus nasoniae gen. nov., sp. nov.' was therefore proposed for the discovered bacterium due to its characteristics and its microbial interaction with N. vitripennis. The type strain of A. nasoniae is Strain SKI4.

Sodalis is a genus of bacteria within the family Pectobacteriaceae. This genus contains several insect endosymbionts and also a free-living group. It is studied due to its potential use in the biological control of the tsetse fly. Sodalis is an important model for evolutionary biologists because of its nascent endosymbiosis with insects.

<span class="mw-page-title-main">Holobiont</span> Host and associated species living as a discrete ecological unit

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Spiroplasma poulsonii are bacteria of the genus Spiroplasma that are commonly endosymbionts of flies. These bacteria live in the hemolymph of the flies, where they can act as reproductive manipulators or defensive symbionts.

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<span class="mw-page-title-main">Morganellaceae</span> Family of bacteria

The Morganellaceae are a family of Gram-negative bacteria that include some important human pathogens formerly classified as Enterobacteriaceae. This family is a member of the order Enterobacterales in the class Gammaproteobacteria of the phylum Pseudomonadota. Genera in this family include the type genus Morganella, along with Arsenophonus, Cosenzaea, Moellerella, Photorhabdus, Proteus, Providencia and Xenorhabdus.

Candidatus Arsenophonus arthropodicus is a Gram-negative and intracellular secondary (S) endosymbiont that belongs to the genus Arsenophonus. This bacterium is found in the Hippoboscid louse fly, Pseudolynchia canariensis. S-endosymbionts are commonly found in distinct tissues. Strains of recovered Arsenophonus found in arthropods share 99% sequence identification in the 16S rRNA gene across all species. Arsenophonus-host interactions involve parasitism and mutualism, including a popular mechanism of "male-killing" found commonly in a related species, Arsenophonus nasoniae. This species is considered "Ca. A. arthropodicus" due it being as of yet uncultured.

References

  1. 1 2 3 LPSN lpsn.dsmz.de
  2. ↑ Gherna, Robert L.; et al. (1991). "NOTES: Arsenophonus nasoniae gen. nov., sp. nov., the Causative Agent of the Son-Killer Trait in the Parasitic Wasp Nasonia vitripennis". International Journal of Systematic Bacteriology. 41 (4): 563–565. doi: 10.1099/00207713-41-4-563 .
  3. ↑ Duron, Olivier; Bouchon, Didier; Boutin, Sébastien; Bellamy, Lawrence; Zhou, Liqin; Engelstädter, Jan; Hurst, Gregory D. (2008-06-24). "The diversity of reproductive parasites among arthropods: Wolbachiado not walk alone". BMC Biology. 6 (1): 27. doi: 10.1186/1741-7007-6-27 . ISSN   1741-7007. PMC   2492848 . PMID   18577218.
  4. ↑ Yañez, Orlando (2016). "Endosymbiotic bacteria in honey bees: Arsenophonus spp. are not transmitted transovarially". FEMS Microbiology Letters. 363 (14): fnw147. doi:10.1093/femsle/fnw147. PMC   4941583 . PMID   27279628.
  5. 1 2 Drew, Georgia C.; Budge, Giles E.; Frost, Crystal L.; Neumann, Peter; Siozios, Stefanos; Yañez, Orlando; Hurst, Gregory D. D. (October 2021). "Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts". The ISME Journal. 15 (10): 2956–2968. Bibcode:2021ISMEJ..15.2956D. doi:10.1038/s41396-021-00977-z. ISSN   1751-7370. PMC   8443716 . PMID   33941888.
  6. ↑ Fan, Hai-Wei; Lu, Jia-Bao; Ye, Yu-Xuan; Yu, Xiao-Ping; Zhang, Chuan-Xi (2016). "Characteristics of the draft genome of "Candidatus Arsenophonus nilaparvatae", a facultative endosymbiont of Nilaparvata lugens". Insect Science. 23 (3): 478–486. Bibcode:2016InsSc..23..478F. doi:10.1111/1744-7917.12318. ISSN   1744-7917. PMID   26792263. S2CID   44398605.
  7. ↑ Nadal-Jimenez, Pol; Griffin, Joanne S.; Davies, Lianne; Frost, Crystal L.; Marcello, Marco; Hurst, Gregory D. D. (2019). "Genetic manipulation allows in vivo tracking of the life cycle of the son-killer symbiont, Arsenophonus nasoniae, and reveals patterns of host invasion, tropism and pathology". Environmental Microbiology. 21 (8): 3172–3182. Bibcode:2019EnvMi..21.3172N. doi:10.1111/1462-2920.14724. ISSN   1462-2920. PMC   6771839 . PMID   31237728.
  8. ↑ Huger, AM; Skinner, SW; Werren, JH (1985). "Bacterial infections associated with the son-killer trait in the parasitoid wasp Nasonia (= Mormoniella) vitripennis (Hymenoptera: Pteromalidae)". Journal of Invertebrate Pathology. 46 (3): 272–80. Bibcode:1985JInvP..46..272H. doi:10.1016/0022-2011(85)90069-2. PMID   4067323.
  9. ↑ Nadal-Jimenez, Pol; Griffin, Joanne S.; Davies, Lianne; Frost, Crystal L.; Marcello, Marco; Hurst, Gregory D. D. (August 2019). "Genetic manipulation allows in vivo tracking of the life cycle of the son-killer symbiont, Arsenophonus nasoniae , and reveals patterns of host invasion, tropism and pathology". Environmental Microbiology. 21 (8): 3172–3182. Bibcode:2019EnvMi..21.3172N. doi:10.1111/1462-2920.14724. PMC   6771839 . PMID   31237728.
  10. ↑ Werren, J. H.; Skinner, S. W.; Huger, A. M. (1986-02-28). "Male-killing bacteria in a parasitic wasp". Science. 231 (4741): 990–992. Bibcode:1986Sci...231..990W. doi:10.1126/science.3945814. ISSN   0036-8075. PMID   3945814.
  11. ↑ Ferree, Patrick M.; Avery, Amanda; Azpurua, Jorge; Wilkes, Timothy; Werren, John H. (2008-09-23). "A Bacterium Targets Maternally Inherited Centrosomes to Kill Males in Nasonia". Current Biology. 18 (18): 1409–1414. Bibcode:2008CBio...18.1409F. doi:10.1016/j.cub.2008.07.093. ISSN   0960-9822. PMC   2577321 . PMID   18804376.
  12. ↑ Engelstädter, Jan; Hurst, Gregory D. D. (January 2007). "The Impact of Male-Killing Bacteria on Host Evolutionary Processes". Genetics. 175 (1): 245–254. doi:10.1534/genetics.106.060921. ISSN   0016-6731. PMC   1774985 . PMID   17151259.
  13. ↑ Hurst, Gregory D. D.; Majerus, Michael E. N. (July 1993). "Why do maternally inherited microorganisms kill males?". Heredity. 71 (1): 81–95. doi: 10.1038/hdy.1993.110 . ISSN   1365-2540. S2CID   26129786.
  14. ↑ Parratt, Steven R.; Frost, Crystal L.; Schenkel, Martijn A.; Rice, Annabel; Hurst, Gregory D. D.; King, Kayla C. (20 June 2016). "Superparasitism Drives Heritable Symbiont Epidemiology and Host Sex Ratio in a Wasp". PLOS Pathogens. 12 (6): e1005629. doi: 10.1371/journal.ppat.1005629 . PMID   27322651.
  15. ↑ Nováková, E.; Hypša, V.; Moran, A. (2009). "Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution". BMC Microbiology. 9: 143. doi: 10.1186/1471-2180-9-143 . PMC   2724383 . PMID   19619300.
  16. ↑ Perotti, M. Alejandra; Allen, Julie M.; Reed, David L.; Braig, Henk R. (April 2007). "Host-symbiont interactions of the primary endosymbiont of human head and body lice". FASEB Journal. 21 (4): 1058–1066. doi: 10.1096/fj.06-6808com . ISSN   1530-6860. PMID   17227954. S2CID   18998241.
  17. ↑ Nováková, Eva; Hypša, Václav; Nguyen, Petr; Husník, Filip; Darby, Alistair C. (2016-09-17). "Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae)". Standards in Genomic Sciences. 11 (1): 72. Bibcode:2016SGenS..11...72N. doi: 10.1186/s40793-016-0195-1 . ISSN   1944-3277. PMC   5027103 . PMID   27660670.
  18. ↑ Budge, Giles E.; Adams, Ian; Thwaites, Richard; Pietravalle, Stéphane; Drew, Georgia C.; Hurst, Gregory D. D.; Tomkies, Victoria; Boonham, Neil; Brown, Mike (November 2016). "Identifying bacterial predictors of honey bee health". Journal of Invertebrate Pathology. 141: 41–44. Bibcode:2016JInvP.141...41B. doi:10.1016/j.jip.2016.11.003. ISSN   1096-0805. PMID   27818181.
  19. ↑ Cornman, R. Scott; Tarpy, David R.; Chen, Yanping; Jeffreys, Lacey; Lopez, Dawn; Pettis, Jeffery S.; vanEngelsdorp, Dennis; Evans, Jay D. (2012-08-21). "Pathogen Webs in Collapsing Honey Bee Colonies". PLOS ONE. 7 (8): e43562. Bibcode:2012PLoSO...743562C. doi: 10.1371/journal.pone.0043562 . ISSN   1932-6203. PMC   3424165 . PMID   22927991.
  20. ↑ Nadal-Jimenez, Pol; Siozios, Stefanos; Frost, Crystal L.; Court, Rebecca; Chrostek, Ewa; Drew, Georgia C.; Evans, Jay D.; Hawthorne, David J.; Burritt, James B.; Hurst, Gregory D. D. (2022-08-03). "Arsenophonus apicola sp. nov., isolated from the honeybee Apis mellifera". International Journal of Systematic and Evolutionary Microbiology. 72 (8). doi:10.1099/ijsem.0.005469. ISSN   1466-5026. PMID   35930469.
  21. ↑ Siozios, Stefanos; Nadal-Jimenez, Pol; Azagi, Tal; Sprong, Hein; Frost, Crystal L.; Parratt, Steven R.; Taylor, Graeme; Brettell, Laura; Liew, Kwee Chin; Croft, Larry; King, Kayla C.; Brockhurst, Michael A.; Hypša, Václav; Novakova, Eva; Darby, Alistair C. (2024-12-16). "Genome dynamics across the evolutionary transition to endosymbiosis". Current Biology. 34 (24): 5659–5670.e7. Bibcode:2024CBio...34.5659S. doi: 10.1016/j.cub.2024.10.044 . ISSN   0960-9822. PMID   39549700.
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