Xue Y et al. (2024) BMC Biol "The marine environmental microbiome mediates physiological outcomes in host nematodes"

Zhang L, Cao X, Xie Y, Xue Y

[BMC Biol, 2024]

Background: Nematodes are the most abundant metazoans in marine sediments, many of which are bacterivores; however, how habitat bacteria affect physiological outcomes in marine nematodes remains largely unknown. RESULTS: Here, we used a Litoditis marina inbred line to assess how native bacteria modulate host nematode physiology. We characterized seasonal dynamic bacterial compositions in L. marina habitats and examined the impacts of 448 habitat bacteria isolates on L. marina development, then focused on HQbiome with 73 native bacteria, of which we generated 72 whole genomes sequences. Unexpectedly, we found that the effects of marine native bacteria on the development of L. marina and its terrestrial relative Caenorhabditis elegans were significantly positively correlated. Next, we reconstructed bacterial metabolic networks and identified several bacterial metabolic pathways positively correlated with L. marina development (e.g., ubiquinol and heme b biosynthesis), while pyridoxal 5'-phosphate biosynthesis pathway was negatively associated. Through single metabolite supplementation, we verified CoQ10, heme b, acetyl-CoA, and acetaldehyde promoted L. marina development, while vitamin B6 attenuated growth. Notably, we found that only four development correlated metabolic pathways were shared between L. marina and C. elegans. Furthermore, we identified two bacterial metabolic pathways correlated with L. marina lifespan, while a distinct one in C. elegans. Strikingly, we found that glycerol supplementation significantly extended L. marina but not C. elegans longevity. Moreover, we comparatively demonstrated the distinct gut microbiota characteristics and their effects on L. marina and C. elegans physiology.Conclusions: Given that both bacteria and marine nematodes are dominant taxa in sedimentary ecosystems, the resource presented here will provide novel insights to identify mechanisms underpinning how habitat bacteria affect nematode biology in a more natural context. Our integrative approach will provide a microbe-nematodes framework for microbiome mediated effects on host animal fitness.

Vancoppenolle B et al. (1996) European Worm Meeting "Comparison of the early embryonic cell lineage of Caenorhabdi- tis elegans and Pellioditis marina, two rhabditid nematodes."

Borgonie G, Coomans AV, Schnabel R, Vancoppenolle B

[European Worm Meeting, 1996]

The early embryonic cell lineage of Pellioditis marina, a marine rhabditid with relatively short developing time was traced using a 4D-microscope. Although the general pattern of cell divisions is congruent with the lineage described for Caenorhabditis elegans by Sulston and coworkers, striking differences can be observed concerning migrations, timing of divisions and cell deaths. The AB, MS and C lineage of P. marina differ from those of C. elegans both in the occurence of additional cell deaths as wel as in the abscence of certain cell deaths. Additionaly, Caap does not divide in accordance with the characteristic period of the rest of the C lineage. In contrast with C. elegans, the E founder cell in P. marina undergoes a migration before gastrulation and devides into Ea and Ep only after E has entered the interior of the embryo. D and P4 divide in a similar way as in C. elegans.

Vancoppenolle B et al. (1997) International C. elegans Meeting "COMPARISON OF THE EMBRYONIC CELL LINEAGE OF CAENORHABDITIS ELEGANS AND PELLIODITIS MARINA"

Vancoppenolle B, Schnabel R, Coomans AV, Borgonie G

[International C. elegans Meeting, 1997]

The early embryonic cell lineage of Pellioditis marina, a marine rhabditid with relatively short developing time (9hrs at 25!C) was traced using a 4D-microscope. Although the general pattern of cell division is congruent with the lineage described for Caenorhabditis elegans by Sulston and Co-workers, striking differences can be observed concerning migrations, timing of divisions and cell deaths. The AB, MS and C lineage of Pellioditis marina differ from those of Caenorhabditis elegans both in the occurence of additional cell deaths as well as in the abscence of certain cell deaths. Additionaly, Caap does not divide in accordance with the characteristic period for the rest of the C-lineage. In contrast with Caenorhabditis elegans, the E founder cell in Pellioditis marina undergoes a migration before gastrulation and divides into Ea and Ep only after E has entered the interior of the embryo. D and P4 divide in a similar way as in Caenorhabditis elegans.

W Houthoofd et al. (2002) European Worm Meeting "Embryonic development of the free-living, marine nematode Pellioditis marina"

K Jacobsen, G Borgonie, B Vancoppenolle, A Coomans, W Houthoofd

[European Worm Meeting, 2002]

Until now only the embryonic cell lineage of the model organism Caenorhabditis elegans has been described (Sulston et al., 1983). The embryonic cell lineage of the free-living nematode Pellioditis marina has been traced from zygote up until the initiation of muscle contraction by means of 4D-microscopy, marking the second detailed description of the embryonic development of a nematode. P. marina is a close relative of C. elegans, but has adapted to a marine, brackish environment. The overall lineage resembles strongly on that of C. elegans, with a few small differences. The developmental tempo of the early embryogenesis (until division of E cell) is more then two times slower than C. elegans. But the primordial germline cell P4 is already present at the 15-cell stage (in C. elegans at the 24-cell stage). At the stage of muscle contraction (when most cells are established), P. marina has as many cells as C. elegans (571 cells) but less cell deaths (67 and 106 respectively). Tissue conservation varies from highly conserved to highly variable. The intestine, the primordial gonad and the body muscles are highly conserved in the two species, while the pharynx, the epidermis and the nervous system have a more variable configuration. The systematic position of Pellioditis remains unsolved, whether Caenorhabditis or Rhabditis is the closest relative. The early embryogenesis and the developmental timing are comparable with that of other Rhabditis species, while the overall cell lineage is almost identical with that of C. elegans. The latter is a strong argument to place P. marina close to C. elegans in the classification. In more primitive nematodes (like Halicephalobus sp.), sublineages form identical cells, which migrate to their exact location. C. elegans has adjusted these lineages to avoid these migrations (Borgonie et al., 2000). This could explain the chaotic' fate topology in the C. elegans cell lineage. P. marina falls in between: it has already adjusted the Caa-lineage to form two nerve cells, but still has migrations that are avoided in C. elegans.

Sudhaus W (1974) Zool. Jb. Syst. Bd. "Zur Systematik, Verbreitung, Okologie und Biologie neuer und wenig bekannter Rhabditiden (Nematoda) 2. Teil."

Sudhaus W

[Zool. Jb. Syst. Bd., 1974]

Five new species of the genus Rhabditis are described (Rh. riemanni n. sp., Rh. remanei n. sp., Rh. reciproca n. sp., Rh. blumi n. sp., and Rh. valida n. sp.) belonging to five subgenera (Crustorhabditis, Caenorhabditis, Rhabditis, Cephaloboides, and Pellioditis). The descriptions of four additional species are revised (Rh. ocypodis Chitwood, Rh. scanica Allgen, Rh. plicata Volk, and Rh. bengalensis Timm). The new subgenus Crustorhabditis n. subgen. derives from the paraphyletic subgenus Mesorhabditis. The species of the former group show a transition from living in littoral seaweed deposits to an obligate association with amphibious crabs (Crustacea). Information about the distribution, ecology, biology and ethology of all these species is presented (with two distribution maps, one for Rh. marina for comparison). Supplementary notes are given from Protorhabditis oxyuroides Sudhaus and Rhabditis tripartita von Linstow.

Ames, Kristina et al. (2017) International Worm Meeting "A Non-Cell-Autonomous Role of BEC-1/BECN1/Beclin1 in Coordinating Cell-Cycle Progression and Stem Cell Proliferation during Germline Development."

Gonzalez, Brenda, Shechter, Gabriel, Starikov, Lev, Konta, Marina, Lin, Feng, Wong, Sara, Da Cunha, Dayse, Ames, Kristina, Melendez, Alicia, Bulow, Hannes

[International Worm Meeting, 2017]

Autophagy is a conserved cellular recycling process crucial for cellular homeostasis. In a multistep process, cellular material destined for degradation is enclosed in an organelle with a double-membrane, the autophagosome, which in turn fuses with the lysosome. BEC-1, the C. elegans ortholog of Beclin1/BECN1 in mammals, was shown to be a haploinsufficient tumor suppressor protein in mammals, crucial for the initial nucleation step of autophagosome formation. In previous studies we showed that BEC-1 serves important functions during development, and longevity of multicellular organisms. In addition, we demonstrated a role for BEC-1 in endocytosis, including in retromer transport from endosome to Golgi, and lipid homeostasis. We now describe a novel role for BEC-1 and autophagy in germ line stem cell homeostasis. The decision of a stem cell to proliferate or differentiate is finely controlled, and several pathways, such as GLP-1/Notch, DAF-2/ insulin IGF-1 receptor (IIR), and DAF-7/TGF beta signaling have been shown to be required for the proper number of germline progenitors. We found that BEC-1, and several other autophagy proteins, such as ATG-18 (in mammals WIPI1/2), ATG-16.2 (in mammals ATG16L) and ATG-7 (in mammals ATG7) are required for the late larval expansion of germline stem cell progenitors during development. Interestingly, BEC-1, ATG-18, and ATG-16.2 act independently of the GLP-1/Notch or DAF-7/TGF beta pathways, but upstream of the DAF-2/insulin IGF-1 receptor (IIR) signaling pathway, to promote germline stem cell proliferation. BEC-1, ATG-18, and ATG-16.2, all promote cell cycle progression and are negatively regulated by DAF-18/PTEN, similar to DAF-2/IIR. However, whereas BEC-1 acts through SKN-1/Nrf1, ATG-18 and ATG-16.2 act through the DAF-16/FOXO transcription factor. In contrast, ATG-7 functions together with the DAF-7/TGF beta pathway, to promote germline proliferation, and is not required for cell cycle progression. Interestingly, BEC-1/Beclin1 functions cell non-autonomously to facilitate cell cycle progression and stem cell proliferation. Thus, our findings demonstrate a novel, non-autonomous role for BEC-1 in the control of stem cell proliferation, and cell cycle progression.

Houthoofd W et al. (2008) Int J Dev Biol "The embryonic cell lineage of the nematode Rhabditophanes sp."

Willems M, Jacobsen K, Borgonie G, Coomans A, Houthoofd W

[Int J Dev Biol, 2008]

One of the unique features of the model organism Caenorhabditis elegans is its invariant development, where a stereotyped cell lineage generates a fixed number of cells with a fixed cell type. It remains unclear how embryonic development evolved within the nematodes to give rise to the complex, invariant cell lineage of C. elegans. Therefore, we determined the embryonic cell lineage of the nematode, Rhabditophanes sp. (family Alloionematidae) and made detailed cell-by-cell comparison with the known cell lineages of C. elegans, Pellioditis marina and Halicephalobus gingivalis. This gave us a unique data set of four embryonic cell lineages, which allowed a detailed comparison between these cell lineages at the level of each individual cell. This lineage comparison revealed a similar complex polyclonal fate distribution in all four nematode species (85% of the cells have the same fate). It is striking that there is a conservation of a C. elegans like polyclonal cell lineage with strong left-right asymmetry. We propose that an early symmetry-breaking event in nematodes of clade IV-V is a major developmental constraint which shapes their asymmetric cell lineage.

Volker Braun et al. (2001) International C. elegans Meeting "Nematode embryonic cell lineages are computationally efficient"

Gaetan Borgonie, Markus Gumbel, Volker Braun, Armand Leroi, Hans-Peter Meinzer, Ricardo Azevedo, Kim Jacobsen, Paul Agapow, Wouter Houthoofd

[International C. elegans Meeting, 2001]

The fixed cell lineages of nematodes like Caenorhabditis elegans are thought to provide a particularly efficient way to build an organism. However, many aspects of the C.elegans embryonic lineage are not obviously efficient (e.g., the distribution of neurons). Here we test whether the embryonic lineages of three species of rhabditid nematodes, C. elegans, Pellioditis marina and Rhabditophanes sp., are computationally efficient in the way cell fates are specified. We define three measures of cell lineage computational efficiency: number of symmetry breaking events, number of determination events and number of sublineages. First, we find that the actual cell lineages of all species specify most cellular phenotypes, such as cell morphology, function, and position in the hatchling, significantly more efficiently than would be expected if these phenotypes were randomly distributed in the same lineage, regardless of the efficiency measure used. Second, we show that the topologies of the actual lineages, themselves, significantly improve the efficiency of cell fate specification compared to cell lineages with random topologies. Third, we find that the cell lineages of the three species, show comparable levels of computational efficiency, despite considerable differences in topology and cell fates assignments. Our results suggest that the embryonic lineages of rhabditid nematodes evolve to place the right cell in the right place in a computationally efficient way.

Ricardo B R Azevedo et al. (2002) East Coast Worm Meeting "Nematode embryonic cell lineages are computationally efficient"

Wouter Houthoofd, Ute Platzer, Volker Braun, Gaetan Borgonie, Armand M Leroi, Kim Jacobsen, Paul-Michael Agapow, Hans-Peter Meinzer, Ricardo B R Azevedo, Markus Gumbel

[East Coast Worm Meeting, 2002]

What is the minimal amount of information required to specify the cells of a metazoan? Based on ideas from algorithmic information theory and phylogenetics, we develop an algorithm for predicting the distribution of determination events in complete cell lineages. We assume that all such events are either cell autonomous or the outcome of permissive cell-cell interactions, and that the lineage is parsimoniously specified. Applying our algorithm to the complete embryonic lineage of Caenorhabditis elegans, we show that it predicts many known molecular events required to specify cell fates. We then show that less information is required to specify the actual C. elegans lineage than lineages simulated under null models. This is also true for two other species of rhabditid nematode, Pellioditis marina and Rhabditophanes sp., despite many interspecific differences in lineage topology and cell fate assignments. Only one cell fate was found to be inneficiently specified in all species: programmed cell death. Unlike normal cells, most apoptotic cells appear to have no particular function during development. However, we show that the computational efficiency of embryonic development would be increased if cell deaths did not occur all. Thus, selection for increased computational efficiency should lead to a reduction in the number of programmed cell deaths in embryonic cell lineages. Although many programmed cell deaths occur in the C. elegans embryonic lineage (17% of all cells), all of them occur in single-cell monoclones. This is a significantly higher proportion than that expected from permuted lineages and suggests that cell deaths have not accumulated neutrally in the cell lineages of the ancestors of C. elegans. That the absence of cell death monoclones containing two or more cells is due to selection and not due to an intrinsic constraint is demonstrated by the observation that they have been found in other species. Such cases, we suggest, arise frequently, but are then eliminated by reprogramming. Indeed, the main function of somatic cell death in these nematodes might be to eliminate redundant cells over the course of evolution. Our results strongly suggest that selection for computational efficiency moulds the evolution of nematode embryonic cell lineages. But even though nematode lineages are more efficient than random lineages, they are clearly not as efficient as they might be. Why not? The polyclonal origin of some cell fates might be due to the need to generate cells of the same type, such as neurons, in various parts of the embryo. This is supported by the observation that in all species studied here, the majority of cells are born close to their final position in the embryo. We speculate that, in C. elegans, P. marina and Rhabditophanes sp., the fitness cost of repeatedly specifying the same cell type may be less than the cost of additional cell migrations.

Marina Ezcurra et al. (2006) European Worm Meeting "Analysis of the Role of npr-1 in Responses to Noxious Stimuli in ASH"

Marina Ezcurra, William R. Schafer, Peter Swoboda, Sunkyung Lee

[European Worm Meeting, 2006]

Marina Ezcurra, Sunkyung Lee, Peter Swoboda and William R. Schafer. Discrimination of favorable and noxious substances is fundamental for survival. The C.elegans polymodal amphid neuron ASH is the primary neuron for detection of aversive stimuli, and mediates avoidance of water-soluble repellents, high osmolarity and mechanical stimuli such as touch on the nose. npr-1 encodes a seven transmembrane receptor related to mammalian neuropeptide Y receptors. As shown by de Bono et al, natural variation at a single amino acid residue of NPR-1 determines whether the nematodes exhibit solitary or social feeding. Solitary strains such as N2 bear the NPR-1 215 V receptor, while social strains bear NPR-1 215F. Previous studies have shown that ASH neurons express the NPR-1 receptor, and since social feeding is mediated by the nociceptive neuron ASH, we investigated whether how the npr-1 genotype might affect ASH sensory responses. Preliminary behavioral experiments performed in the lab show that npr-1 mutants have higher sensitivity to the repellents glycerol and copper, indicating that the lower NPR-1 activity in 215F might result in higher sensitivity to noxious stimuli. We are carrying out additional behavioral experiments to explore the role of npr-1 in response to noxious stimuli, and using calcium imaging to investigate the role of npr-1 in aversive detection in ASH.. In addition to ASH, ASK and ADL also play roles in detection of chemical repellents. ASK is particularly interesting as it mediates both attractive and repulsive behaviors in C. elegans, but it is not yet know how this polymodality is mediated. Several genes expressed in ASK, such as the TRPV channel osm-9, the soluble cyclic nucleotide gated channel subunit tax-4, and the GPCR alpha subunits gpa-3 and odr-3, are known to be involved in sensory transduction. To test the role of these and other genes in ASK, we have generated a transgenic cameleon line expressed under an ASK specific promoter. This line will be used for calcium imaging to monitor the responses of ASK in mutants of the candidate genes.