The cyanobacterial endosymbiont of the unicellular algae Rhopalodia gibba shows reductive genome evolution
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Background: Bacteria occur in facultative association and intracellular symbiosis with a diversity of eukaryotic hosts. Recently, we have helped to characterise an intracellular nitrogen fixing bacterium, the so-called spheroid body, located within the diatom Rhopalodia gibba. Spheroid bodies are of cyanobacterial origin and exhibit features that suggest physiological adaptation to their intracellular life style. To investigate the genome modifications that have accompanied the process of endosymbiosis, here we compare gene structure, content and organisation in spheroid body and cyanobacterial genomes. Results: Comparison of the spheroid body's genome sequence with corresponding regions of near free-living relatives indicates that multiple modifications have occurred in the endosymbiont's genome. These include localised changes that have led to elimination of some genes. This gene loss has been accompanied either by deletion of the respective DNA region or replacement with non-coding DNA that is AT rich in composition. In addition, genome modifications have led to the fusion and truncation of genes. We also report that in the spheroid body's genome there is an accumulation of deleterious mutations in genes for cell wall biosynthesis and processes controlled by transposases. Interestingly, the formation of pseudogenes in the spheroid body has occurred in the presence of intact, and presumably functional, rec A and rec F genes. This is in contrast to the situation in most investigated obligate intracellular bacterium-eukaryote symbioses, where at least either rec A or rec F has been eliminated. Conclusion: Our analyses suggest highly specific targeting/loss of individual genes during the process of genome reduction and establishment of a cyanobacterial endosymbiont inside a eukaryotic cell. Our findings confirm, at the genome level, earlier speculation on the obligate intracellular status of the spheroid body in Rhopalodia gibba. This association is the first example of an obligate cyanobacterial symbiosis involving nitrogen fixation for which genomic data are available. It represents a new model system to study molecular adaptations of genome evolution that accompany a switch from free-living to intracellular existence.
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A diatom species has been characterized that has endosymbiosed a nitrogen-fixing cyanobacterium, suggesting such relationships are beneficial to at least one of the two species.
“recently, a diatom species has been characterized, which has endosymbiosed a nitrogen-fixing cyanobacterium, suggesting that such relationships are indeed beneficial to at least one of the two species [104,105]”
From Biofuels from algae: Challenges and potential (2010) · cites this paper as [104]
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“gibba spheroid body uncovered remnants of genes for photosynthesis, in addition to a complete set of N2fixation enzymes (Kneip et al. 2008).”
BackgroundMoal, M. L., Collin, H., & Biegala, I. C. (2011) · Biogeosciences · doi:10.5194/bg-8-827-2011 · Cited by 40 · see citing works
Evolutionary genomic insights into cyanobacterial symbioses in plants
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“Data on T. azolla and the nitrogen-fixing cyanobionts of the diatoms Rhopalodia gibba , UCYN-A (a symbiont of a haptophyte) and Epithemia turgida all point towards genome erosion (Kneip et al., 2008; Nakayama et al., 2014; Ran et al., 2010).”
Review: origin of complex algae by secondary endosymbiosis: a journey through time
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“Moreover, apart from Paulinella, there are many other eukaryotes in endosymbiotic relationships with cyanobacteria [140–143].”
BackgroundGenomic divergence within non-photosynthetic cyanobacterial endosymbionts in rhopalodiacean diatoms
Nakayama, T., & Inagaki, Y. (2017) · Scientific Reports · doi:10.1038/s41598-017-13578-8 · Cited by 36 · see citing works
Physiology, anaerobes, and the origin of mitosing cells 50 years on
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Toward an empirical framework for interpreting plastid evolution
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“Beyond these well-characterized cases, a diversity of endosymbioses have achieved varied levels of integration, ranging from transitory kleptoplasty to some that arguably have reached the status of incipient organelles (Nakabachi et al. 2006, Tamames et al. 2007, Kneip et al. 2008, Ran et al. 2010).”
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Origins of Mitochondria and Plastids
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“Cyanobacterial interactions with plants and protists are also well known and in most cases the associations are facultative, without any vertical transmission (Kneip et al., 2008).”
BackgroundAzolla: A Model System for Symbiotic Nitrogen Fixation and Evolutionary Developmental Biology
de Vries, S., & de Vries, J. (2018) · Springer eBooks · doi:10.1007/978-3-319-75103-0_2 · Cited by 29 · see citing works
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“Overall, the diazoplasts of Epithemia diatoms are an ideal case study for both the acquisition of nitrogen fixation function by a photosynthetic eukaryote and investigating evolution associated with endosymbiotic organellogenesis [19].”
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“Of special interest are the new candidates for organellogenesis such as the cyanobacterial-type resident of Rhopalodia gibba diatom [50], the psyllid endosymbiont Carsonella ruddii [51], and, in particular, the nuclear genome of P.”
BackgroundCyanobacteria in Nitrogen-Fixing Symbioses
Bustos‐Díaz, E. D., Barona‐Gómez, F., & Cibrián‐Jaramillo, A. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-814667-5.00002-7 · Cited by 19 · see citing works
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“2004) and show many modifications in their genome typical of other endosymbionts, such as numerous deletions, elevated AT content, loss/fusion/truncation of genes, pseudogenization, and expansion of non-coding regions (Prechtl et al. 2004; Kneip et al. 2008).”
BackgroundRhopalodia gibba: The First Steps in the Birth of a Novel Organelle?
Adler, S., Trapp, E. M., Dede, C., Maier, U. G., & Zauner, S. (2013) · Springer eBooks · doi:10.1007/978-3-7091-1303-5_9 · Cited by 14 · see citing works
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Diatom Symbioses with Other Photoautotroph
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Cellular compartmentation follows rules: The Schnepf theorem, its consequences and exceptions
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“tained, which is thought to have provided fixed nitrogen, hence favoring the cellular merger [52, 53].”
BackgroundSelf-citationMetabolic compatibility and the rarity of prokaryote endosymbioses
Libby, E., Kempes, C. P., & Okie, J. G. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2206527120 · Cited by 10 · see citing works
“If, instead, we consider only intracellular endosymbionts which can be found in both multicellular and unicellular eukaryotes [57, 58, 11, 62, 63, 64], then many of these also involve specialized spaces, e.”
BackgroundUnique genome evolution in an intracellular N2-fixing symbiont of a rhopalodiacean diatom
Nakayama, T., & Inagaki, Y. (2014) · Acta Societatis Botanicorum Poloniae · doi:10.5586/asbp.2014.046 · Cited by 10 · see citing works
“gibba spheroid body genome [15], the EtSB also contains the complete nif gene cluster, with the exception of fdxN and nifU (discussed in the following section).”
BackgroundResultInfluentialHarnessing Solar‐Powered Oxic N 2 ‐fixing Cyanobacteria for the BioNitrogen Economy
Young, J. S., Gu, L., Gibbons, W. R., & Zhou, R. (2021) · doi:10.1002/9783527824908.ch13 · Cited by 9 · see citing works
Synthetic threads through the web of life
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“While other nitrogen-fixing cyanobacteria synthesize nitrogen-bearing toxins, Epithemia’s endosymbionts synthesize all 23 essential amino acids required by animals (68), despite genome reduction that eliminated both photosystems (68, 69).”
BackgroundThe Photosynthetic Apparatus of the Living Fossil, Cyanophora paradoxa
Steiner, J. M., & Löffelhardt, W. (2011) · Springer eBooks · doi:10.1007/978-94-007-0388-9_2 · Cited by 7 · see citing works
“…ancestor, estimated age 60 My) are surrounded by two membranes only, whereas the nitrogen-fixing spheroid bodies from the diatom Rhopalodia gibba (Kneip et al. 2008; derived from a Cyanothece-like cyanobacterium, estimated age 25–35 My) are still surrounded by three membranes (Kovacevic et al.…”
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“The remaining five and three sequences were grouped with Cyanothece ATCC51142 and the endosymbiont of Rhopalodia gibba, respectively.”
BackgroundInfluentialTesting Nanomaterial Toxicity in Unicellular Eukaryotic Algae and Fish Cell Lines
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BackgroundInfluentialPrice, D. C., Steiner, J. M., Yoon, H. S., Bhattacharya, D., & Löffelhardt, W. (2016) · Springer eBooks · doi:10.1007/978-3-319-32669-6_42-1 · Cited by 4 · see citing works
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Integrative taxonomy, whole organelle genomes and endosymbiosis in Rhopalodia sterrenburgii Krammer
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“This phenomenon has already been well-documented in diatom spheroid bodies, particularly within various lineages of the order Rhopalodiales (Kneip et al., 2008; Nakayama et al., 2014; Nakayama and Inagaki, 2017; Schvarcz et al., 2024).”
Effects and Dynamics of Insertion Sequences in the Evolution of Cyanobacteria
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Cyanobacterial and Algal Symbioses
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“8% for the 507 region spanning the nif operon[54] (Kniep et al.”
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Using systems biology to exploit the resources/natural reservoirs for biofuel production
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Review: Evolutionary genomic insights into cyanobacterial symbioses in plants — R0/PR2
(2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr2
Review: Evolutionary genomic insights into cyanobacterial symbioses in plants — R1/PR6
(2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr6
Author comment: Evolutionary genomic insights into cyanobacterial symbioses in plants — R1/PR5
de Vries, S. (2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr5
Recommendation: Evolutionary genomic insights into cyanobacterial symbioses in plants — R0/PR3
(2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr3
Author comment: Evolutionary genomic insights into cyanobacterial symbioses in plants — R0/PR1
de Vries, S. (2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr1
Decision: Evolutionary genomic insights into cyanobacterial symbioses in plants — R0/PR4
(2021) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr4
Decision: Evolutionary genomic insights into cyanobacterial symbioses in plants — R2/PR11
(2022) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr11
Recommendation: Evolutionary genomic insights into cyanobacterial symbioses in plants — R1/PR7
(2022) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr7
Author comment: Evolutionary genomic insights into cyanobacterial symbioses in plants — R2/PR9
de Vries, S. (2022) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr9
Recommendation: Evolutionary genomic insights into cyanobacterial symbioses in plants — R2/PR10
(2022) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr10
Decision: Evolutionary genomic insights into cyanobacterial symbioses in plants — R1/PR8
(2022) · Quantitative Plant Biology · doi:10.1017/qpb.2022.3.pr8
Büdel, B. (2024) · Springer eBooks · doi:10.1007/978-3-662-65712-6_6
Bioinformatic investigations in marine microbial ecology
Heller, P. (2014) · eScholarship (California Digital Library)
Chang, A. C. G., Abresch, H. E., Amaral, M. W. W., Keepers, K. G., Greenwood, M., Li, J., Hamsher, S. E., Miller, S. R., & Kociolek, J. P. (2026) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2026.1771974
A symbiogenic merger enabled by oxygen initiated the evolution of eukaryotes
Speijer, D. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2620770123
- Authors
- Kneip, C., Voβ, C., Lockhart, P. J., & Maier, U. G.
- Affiliations
- Philipps University of Marburg (DE)
- Allan Wilson Centre (NZ)
- Corresponding author
- Maier, Uwe G
- Venue
- BMC Evolutionary Biology
- Published
- 2008-01-28
- Volume
- 8
- Issue
- 1
- Pages
- 30-30
- ISSN
- 1471-2148 (ISSN-L)
- PMC
- PMC2246100
- OpenAlex
- W2045066585
- Cited by
- 94
- References
- 41
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 4 · 2023: 4 · 2022: 7 · 2021: 8 · 2019: 5 · 2018: 6 · 2017: 6 · 2016: 4 · 2015: 3 · 2014: 7 · 2013: 5 · 2012: 7
- FWCI
- 3.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- BMC Evolutionary Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Max Planck Institute for Plasma Physics (submittedVersion, other-oa)
- Funders
- Alexander von Humboldt-Stiftung
- Deutsche Forschungsgemeinschaft (TP B9)
- Marsden Fund
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Keywords
- spheroid bodies, cyanobacterial endosymbiont, intracellular symbiosis, genome reduction, gene loss, pseudogenes, RecA, recF, transposase, deleterious mutations, gene fusion, nitrogen fixation, diatoms, obligate intracellular bacteria
- MeSH terms
- Bacterial Proteins, Cloning, Molecular, DNA-Binding Proteins, Nitrogen Fixation, Operon, Phylogeny, Pseudogenes, Rec A Recombinases, Sequence Homology, Nucleic Acid, Symbiosis, Genome, Bacterial, Gene Deletion, Diatoms, Algal Proteins, Cyanothece
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