Bacterial Symbiosis Maintenance in the Asexually Reproducing and Regenerating Flatworm Paracatenula galateia

Dirks, Ulrich; Gruber‐Vodicka, Harald R.; Leisch, Nikolaus; Bulgheresi, Silvia; Egger, Bernhard; Ladurner, Peter; Ott, Jörg

doi:10.1371/journal.pone.0034709

Cited by 31 publications

(31 citation statements)

References 66 publications

(97 reference statements)

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“…In M. lignano , the cell migration of BrdU-labelled cells is about 6.5 μm per hour [ 26 ], similar to the 5 μm per hour we found for Monocelis sp. In catenulids, no migration speed was determined, but judging from the figures given in [ 27 , 28 ] using the same method described in this paper, the migration speed is about 4.7 μm per hour ( n = 3).…”

Section: Discussionmentioning

confidence: 99%

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Girstmair

Schnegg

Telford

et al. 2014

EvoDevo

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BackgroundProseriates (Proseriata, Platyhelminthes) are free-living, mostly marine, flatworms measuring at most a few millimetres. In common with many flatworms, they are known to be capable of regeneration; however, few studies have been done on the details of regeneration in proseriates, and none cover cellular dynamics. We have tested the regeneration capacity of the proseriate Monocelis sp. by pre-pharyngeal amputation and provide the first comprehensive picture of the F-actin musculature, serotonergic nervous system and proliferating cells (S-phase in pulse and pulse-chase experiments and mitoses) in control animals and in regenerates.ResultsF-actin staining revealed a strong body wall, pharynx and dorsoventral musculature, while labelling of the serotonergic nervous system showed an orthogonal pattern and a well developed subepidermal plexus. Proliferating cells were distributed in two broad lateral bands along the anteroposterior axis and their anterior extension was delimited by the brain. No proliferating cells were detected in the pharynx or epidermis.Monocelis sp. was able to regenerate the pharynx and adhesive organs at the tip of the tail plate within 2 or 3 days of amputation, and genital organs within 8 to 10 days. Posterior pieces were not able to regenerate a head.The posterior regeneration blastema was found to be a centre of cell proliferation, whereas within the pharynx primordium, little or no proliferation was detected. The pharynx regenerated outside of the blastema and was largely, but not solely formed by cells that were proliferating at the time of amputation.ConclusionsOur findings suggest that proliferating cells or their offspring migrated to the place of organ differentiation and then stopped proliferating at that site. This mode of rebuilding organs resembles the mode of regeneration of the genital organs in another flatworm, Macrostomum lignano. Pharynx regeneration resembles embryonic development in Monocelis fusca and hints at the vertically directed pharynx being plesiomorphic in proseriates.Proliferation within the regeneration blastema has been detected in anterior and posterior blastemas of other flatworms, but is notably missing in triclads. The phylogenetic relationships of the flatworms studied indicate that proliferation within the blastema is the plesiomorphic condition in Platyhelminthes.Electronic supplementary materialThe online version of this article (doi:10.1186/2041-9139-5-37) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Girstmair

Schnegg

Telford

et al. 2014

EvoDevo

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“…In most organisms, chromatoid bodies are germ‐cell‐specific cytoplasmic structures for RNA processing (Kotaja and Sassone‐Corsi, ). In flatworms, chromatoid bodies have also been described in neoblast stem cells of triclads (Hori, ), polyclads (Sato et al, ), macrostomorphans (Ladurner et al, ) and catenulids (Dirks et al, ). Here, we describe for the first time chromatoid bodies in male germ cells of a polyclad flatworm (Figures B and 3E).…”

Section: Discussionmentioning

confidence: 99%

Ultrastructure of spermatogenesis and mature spermatozoa in the flatworm Prosthiostomum siphunculus (Polycladida, Cotylea)

Gammoudi

Salvenmoser

Harrath

et al. 2015

Cell Biology International

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This is the first study investigating spermatogenesis and spermatozoan ultrastructure in the polyclad flatworm Prosthiostomum siphunculus. The testes are numerous and scattered as follicles ventrally between the digestive ramifications. Each follicle contains the different stages of sperm differentiation. Spermatocytes and spermatids derive from a spermatogonium and the spermatids remain connected by intercellular bridges. Chromatoid bodies are present in the cytoplasm of spermatogonia up to spermatids. During early spermiogenesis, a differentiation zone appears in the distal part of spermatids. A ring of microtubules extends along the entire sperm shaft just beneath the cell membrane. An intercentriolar body is present and gives rise to two axonemes, each with a 9 þ "1" micro-tubular pattern. Development of the spermatid leads to cell elongation and formation of a filiform, mature spermatozoon with two free flagella and with cortical microtubules along the sperm shaft. The flagella exit the sperm shaft at different levels, a finding common for acotyleans, but so far unique for cotylean polyclads. The Golgi complex produces numerous electron-dense bodies of two types and of different sizes. These bodies are located around a perinuclear row of mitochondria. The elongated nucleus extends almost along the entire sperm body. The nucleus is wide in the proximal part and becomes narrow going towards the distal end. Thread-like chromatin mixed with electron-dense intranuclear spindle-shaped bodies are present throughout nucleus. The general sperm ultrastructure, the presence of intranuclear bodies and a second type of cytoplasmic electron-dense bodies may provide characters useful for phylogenetic analysis.

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“…As more knowledge is gained about host and symbiont genomics, and we learn how symbiont and host genes function, answers to these questions will be forthcoming. [22] . B) Cyanobacterial plant leaf nodule symbionts are transmitted vertically by colonizing the apical and axillary bud tissue after germination, from which they colonize either vegetative shoots or reproductive shoots [105] .…”

Section: Discussionmentioning

confidence: 99%

A Symbiont’s Guide to the Germline

Russell

Chappell

Sullivan

2019

Preprint

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Microbial symbioses exhibit astounding adaptations, yet all symbionts face the problem of how to reliably associate with host offspring every generation. A common strategy is vertical transmission, in which symbionts are directly transmitted from the female to her offspring. The diversity of symbionts and vertical transmission mechanisms is as expansive as the diversity of eukaryotic host taxa that house them. However, there are several common themes among these mechanisms based on the degree to which symbionts associate with the host germline during transmission. In this review, we detail three distinct vertical transmission strategies, starting with associations that are transmitted from host somatic cells to offspring somatic cells, either due to lacking a germline or avoiding it. A second strategy involves somatically-localized symbionts that migrate into the germline during host development. The third strategy we discuss is one in which the symbiont maintains continuous association with the germline throughout development. Unexpectedly, the vast majority of documented vertically inherited symbionts rely on the second strategy: soma-to-germline migration. Given that not all eukaryotes contain a sequestered germline and instead produce offspring from somatic stem cell lineages, this soma-to-germline migration is discussed in the context of multicellular evolution. Lastly, as recent genomics data have revealed an abundance of horizontal gene transfer events from symbiotic and non-symbiotic bacteria to host genomes, we discuss their impact on eukaryotic host evolution.

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Bacterial Symbiosis Maintenance in the Asexually Reproducing and Regenerating Flatworm Paracatenula galateia

Cited by 31 publications

References 66 publications

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Ultrastructure of spermatogenesis and mature spermatozoa in the flatworm Prosthiostomum siphunculus (Polycladida, Cotylea)

A Symbiont’s Guide to the Germline

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Bacterial Symbiosis Maintenance in the Asexually Reproducing and Regenerating Flatworm Paracatenula galateia

Cited by 31 publications

References 66 publications

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Cellular dynamics during regeneration of the flatworm Monocelissp. (Proseriata, Platyhelminthes)

Ultrastructure of spermatogenesis and mature spermatozoa in the flatworm Prosthiostomum siphunculus (Polycladida, Cotylea)

A Symbiont&rsquo;s Guide to the Germline

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A Symbiont’s Guide to the Germline