Phagocytosis-like Cell Engulfment by a Planctomycete Bacterium

Overview

Journal Nat Commun

Specialty Biology

Date 2019 Dec 13

PMID 31827088

Citations 26

Authors

Takashi Shiratori

Shigekatsu Suzuki

Yukako Kakizawa

Ken-Ichiro Ishida

Affiliations

Soon will be listed here.

Abstract

Phagocytosis is a key eukaryotic feature, conserved from unicellular protists to animals, that enabled eukaryotes to feed on other organisms. It could also be a driving force behind endosymbiosis, a process by which α-proteobacteria and cyanobacteria evolved into mitochondria and plastids, respectively. Here we describe a planctomycete bacterium, 'Candidatus Uab amorphum', which is able to engulf other bacteria and small eukaryotic cells through a phagocytosis-like mechanism. Observations via light and electron microscopy suggest that this bacterium digests prey cells in specific compartments. With the possible exception of a gene encoding an actin-like protein, analysis of the 'Ca. Uab amorphum' genomic sequence does not reveal any genes homologous to eukaryotic phagocytosis genes, suggesting that cell engulfment in this microorganism is probably not homologous to eukaryotic phagocytosis. The discovery of this "phagotrophic" bacterium expands our understanding of the cellular complexity of prokaryotes, and may be relevant to the origin of eukaryotic cells.

Citing Articles

Comparative genomic analyses of aerobic planctomycetes isolated from the deep sea and the ocean surface.

Ovreas L, Kallscheuer N, Calisto R, Bordin N, Storesund J, Jogler C Antonie Van Leeuwenhoek. 2024; 118(1):33.

PMID: 39585435 PMC: 11588811. DOI: 10.1007/s10482-024-02041-0.

Exploring the organic nature, morphological plasticity and ecological significance of Aster like nanoparticles.

Fuster M, Billard H, Mathurin J, Deniset-Besseau A, Albertini D, Sime-Ngando T Sci Rep. 2024; 14(1):22107.

PMID: 39333779 PMC: 11436848. DOI: 10.1038/s41598-024-73332-9.

The emerging view on the origin and early evolution of eukaryotic cells.

Vosseberg J, van Hooff J, Kostlbacher S, Panagiotou K, Tamarit D, Ettema T Nature. 2024; 633(8029):295-305.

PMID: 39261613 DOI: 10.1038/s41586-024-07677-6.

The Last Universal Common Ancestor of Ribosome-Encoding Organisms: Portrait of LUCA.

Forterre P J Mol Evol. 2024; 92(5):550-583.

PMID: 39158619 DOI: 10.1007/s00239-024-10186-9.

An untargeted cultivation approach revealed Pseudogemmatithrix spongiicola gen. nov., sp. nov., and sheds light on the gemmatimonadotal mode of cell division: binary fission.

Haufschild T, Kallscheuer N, Hammer J, Kohn T, Kabuu M, Jogler M Sci Rep. 2024; 14(1):16764.

PMID: 39034380 PMC: 11271474. DOI: 10.1038/s41598-024-67408-9.

References

Sanchez-Amat A, Torrella F . Formation of stable bdelloplasts as a starvation-survival strategy of marine bdellovibrios. Appl Environ Microbiol. 1990; 56(9):2717-25. PMC: 184833. DOI: 10.1128/aem.56.9.2717-2725.1990. View

Yu N, Wagner J, Laird M, Melli G, Rey S, Lo R . PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics. 2010; 26(13):1608-15. PMC: 2887053. DOI: 10.1093/bioinformatics/btq249. View

Crossman L, Chen H, Cerdeno-Tarraga A, Brooks K, Quail M, Pineiro S . A small predatory core genome in the divergent marine Bacteriovorax marinus SJ and the terrestrial Bdellovibrio bacteriovorus. ISME J. 2012; 7(1):148-60. PMC: 3526173. DOI: 10.1038/ismej.2012.90. View

Sagulenko E, Morgan G, Webb R, Yee B, Lee K, Fuerst J . Structural studies of planctomycete Gemmata obscuriglobus support cell compartmentalisation in a bacterium. PLoS One. 2014; 9(3):e91344. PMC: 3954628. DOI: 10.1371/journal.pone.0091344. View

Embley T, Williams T . Evolution: Steps on the road to eukaryotes. Nature. 2015; 521(7551):169-70. DOI: 10.1038/nature14522. View

Cherry J, Hong E, Amundsen C, Balakrishnan R, Binkley G, Chan E . Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 2011; 40(Database issue):D700-5. PMC: 3245034. DOI: 10.1093/nar/gkr1029. View

Stephens R, Kalman S, Lammel C, Fan J, Marathe R, Aravind L . Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis. Science. 1998; 282(5389):754-9. DOI: 10.1126/science.282.5389.754. View

Pearson A, Budin M, Brocks J . Phylogenetic and biochemical evidence for sterol synthesis in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci U S A. 2003; 100(26):15352-7. PMC: 307571. DOI: 10.1073/pnas.2536559100. View

Pollard T, Cooper J . Actin, a central player in cell shape and movement. Science. 2009; 326(5957):1208-12. PMC: 3677050. DOI: 10.1126/science.1175862. View

10.

Lake J, Rivera M . Was the nucleus the first endosymbiont?. Proc Natl Acad Sci U S A. 1994; 91(8):2880-1. PMC: 43475. DOI: 10.1073/pnas.91.8.2880. View

11.

Tocheva E, Matson E, Morris D, Moussavi F, Leadbetter J, Jensen G . Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation. Cell. 2011; 146(5):799-812. PMC: 3176627. DOI: 10.1016/j.cell.2011.07.029. View

12.

Moser R, Aktas M, Fritz C, Narberhaus F . Discovery of a bifunctional cardiolipin/phosphatidylethanolamine synthase in bacteria. Mol Microbiol. 2014; 92(5):959-72. DOI: 10.1111/mmi.12603. View

13.

Xu P, Widmer G, Wang Y, Ozaki L, Alves J, Serrano M . The genome of Cryptosporidium hominis. Nature. 2004; 431(7012):1107-12. DOI: 10.1038/nature02977. View

14.

Yu C, Chen Y, Lu C, Hwang J . Prediction of protein subcellular localization. Proteins. 2006; 64(3):643-51. DOI: 10.1002/prot.21018. View

15.

Boedeker C, Schuler M, Reintjes G, Jeske O, van Teeseling M, Jogler M . Determining the bacterial cell biology of Planctomycetes. Nat Commun. 2017; 8:14853. PMC: 5394234. DOI: 10.1038/ncomms14853. View

16.

Katoh K, Standley D . MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4):772-80. PMC: 3603318. DOI: 10.1093/molbev/mst010. View

17.

Jenkins C, Kedar V, Fuerst J . Gene discovery within the planctomycete division of the domain Bacteria using sequence tags from genomic DNA libraries. Genome Biol. 2002; 3(6):RESEARCH0031. PMC: 116728. DOI: 10.1186/gb-2002-3-6-research0031. View

18.

Martin W, Garg S, Zimorski V . Endosymbiotic theories for eukaryote origin. Philos Trans R Soc Lond B Biol Sci. 2015; 370(1678):20140330. PMC: 4571569. DOI: 10.1098/rstb.2014.0330. View

19.

Goldberg T, Hecht M, Hamp T, Karl T, Yachdav G, Ahmed N . LocTree3 prediction of localization. Nucleic Acids Res. 2014; 42(Web Server issue):W350-5. PMC: 4086075. DOI: 10.1093/nar/gku396. View

20.

Amann R, Binder B, Olson R, Chisholm S, Devereux R, Stahl D . Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol. 1990; 56(6):1919-25. PMC: 184531. DOI: 10.1128/aem.56.6.1919-1925.1990. View