Giant Bacteria

Abstract

For almost all bacteria, it is convenient to be very small, but a few highly specialist groups of bacteria have evolved to be orders of magnitude larger than ordinary bacteria. While some of these giant microbes are abnormally large in all dimensions, others are long and thin or consist of assemblages of multiple cells. These giant bacteria are spread across the domain Bacteria and have evolved multiple ways to combat diffusion constrains. Giant bacteria often thrive in nutrient and carbon‐rich environments and/or in steep redox gradients. Genomically, giant bacteria seem all to be polyploid, that is containing multiple copies of their genome. Giant bacteria have been described throughout the history of microbial research but only some of them can be traced in current taxonomy and are being actively studied. Therefore, it is likely there are other giant bacteria in nature, awaiting to be explored.

Key Concepts

  • Growth and activity of giant bacteria are expected to be constrained by a combination of diffusion of nutrients into the cells as well as intracellular trafficking of solutes by diffusion.
  • Giant bacteria can be divided into ‘truly’ giant, consisting of abnormally large cells on all dimensions, or ‘pseudo‐giant’ consisting of cells abnormally large on one axis or multicellular assemblages of bacteria.
  • ‘Pseudo‐giant’ bacteria may not face the same diffusion limitations as ‘truly’ giant bacteria.
  • ‘Truly’ giant bacteria likely ‘resolve’ diffusion constrains by one or more methods including, minimising cytoplasmic space by intracellular (pseudo)compartmentalisation, storage vacuoles, rapid swimming.
  • Giant bacteria often grow in carbon‐ and nutrient‐rich environments and/or in steep redox gradients, thus additionally minimising diffusion‐related constraints.
  • Current knowledge suggests that all giant bacteria contain multiple copies of their genomes being oligoploid (3–10 copies) or polyploid (10–1000s of copies).
  • Gigantism in bacteria occurs in multiple phylogenetic lineages covering both Gram‐negative and Gram‐positive taxa.
  • Early descriptions of giant bacteria suggest that the currently studied taxa do not encompass the entire diversity of abnormally large bacteria.

Keywords: Spirochaetes; Epulopiscium; Cyanobacteria; sulfur bacteria; cable bacteria; diffusion; polyploidy; ‘truly’ giant bacteria; pseudo‐giant bacteria

Figure 1. A bundle of Thioploca filaments from marine sediments close to the Peruvian coast. The bundle is placed next to a ruler of 5 cm in length. The Thioploca filaments appear white due to internal sulfur granules that reflect the light.
Figure 2. Large intestinal symbionts of surgeonfish. These panels, all shown at the same magnification, illustrate the morphological diversity of ‘Epulopiscium’ and its relatives. The cell on the left is the second largest morphotype, Epulopiscium type B. Visible are two large internal offspring cells. Other rod‐shaped and filamentous forms are shown. Scale bar represents 20 μm (Angert, ). The enigmatic cytoarchitecture of Epulopiscium spp. Reproduced with permission from Fuerst . © Springer Nature.
Figure 3. Examples of large‐celled Cyanobacteria. All scale bars are 10 μm. (a) Chroococcus sp., dividing (left) and recently divided cells from this typically freshwater genus. (b) Porphirosiphon notarissi, a filamentous cyanobacterium allied to the large Oscillatoria, isolated from a soil crust in the Namibian desert, displaying the typical disc‐shaped cells in two separate trichomes, enclosed in a common extracellular sheath. Note the apoptotic, vestigial cell between the two trichomes that served to separate them in a process of self‐immolation. (c) Detail of a morphologically complex Stigonema spp. displaying a main filament consisting of two series of cells, and an incipient uniseriate branch.
Figure 4. The morphology of the giant sulfur bacteria as they appear in the light microscope: (a) Beggiatoa, (b) Thioploca, (c) Thiothrix, (d) Thiomargarita, (e) Thiovulum, (f) Achromatium. In (a–e), numerous sulfur inclusions can be seen. Achromatium (f) is the only known bacterium with calcite inclusions. The scale bars show typical sizes for each genus. Nevertheless, the cell diameters of sulfur bacteria are highly variable.
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References

Agusti S and Phlips EJ (1992) Light absorption by Cyanobacteria: Implications of the colonial growth form. Limnology and Oceanography 37 (2): 434–441. DOI: 10.4319/lo.1992.37.2.0434.

Angert ER and Losick RM (1998) Propagation by sporulation in the guinea pig symbiont Metabacterium polyspora. Proceedings of the National Academy of Sciences of the United States of America 95 (17): 10218–10223. Available at: http://www.ncbi.nlm.nih.gov/pubmed/9707627 (Accessed 29 March 2019).

Angert ER (2006) The enigmatic cytoarchitecture of Epulopiscium spp. In: Shively JM (ed.) Complex Intracellular Structures in Prokaryotes, pp 285–301. Springer: Berlin, Heidelberg. DOI: 10.1007/7171_027.

Bauermeister J, Ramette A and Dattagupta S (2012) Repeatedly evolved host‐specific ectosymbioses between sulfur‐oxidizing bacteria and amphipods living in a cave ecosystem (M Horn, ed.). PLoS ONE 7 (11): e50254. DOI: 10.1371/journal.pone.0050254.

Berlanga M, Paster BJ and Guerrero R (2007) Coevolution of symbiotic spirochete diversity in lower termites. International Microbiology 10 (2): 133–139. DOI: 10.2436/20.1501.01.19.

Chatton E and Perard C (1913) Schizophytes du caecum du cobaye. II Metabacterium polyspora n. g., n. s. Compendes Rendus Hebdomadaires Societe de Biologie (Paris) 74: 1232–1234.

Clarke KJ, Finlay BJ, Vicente E, Lloréns H and Miracle MR (1993) The complex life‐cycle of a polymorphic prokaryote epibiont of the photosynthetic bacterium Chromatium weissei. Archives of Microbiology 159 (6): 498–505. DOI: 10.1007/BF00249026.

Cornejo E, Abreu N and Komeili A (2014) Compartmentalization and organelle formation in bacteria. Current Opinion in Cell Biology 26 (1): 132–138. DOI: 10.1016/j.ceb.2013.12.007.

Delaporte B (1963) Une phénomène singulier des spores mobiles chez des grandes bacteries. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences 5 (257): 1414–1417.

Delaporte B (1970) Etude de la structure, et plus specialement de l'appareil nucleaire, de tres grandes bacteries sporulantes. Zeitschrift für Allgemeine Mikrobiologie 10 (3): 165–182.

Esteve I, Gaju N, Mir J and Guerrero R (1992) Comparison of techniques to determine the abundance of predatory bacteria attacking Chromatiaceae. FEMS Microbiology Letters 86 (86): 205–211. DOI: 10.1016/0378‐1097(92)90783‐K.

Fishelson L, Montgomery WL and Myrberg AA (1985) A unique symbiosis in the gut of tropical herbivorous surgeonfish (Acanthuridae: teleostei) from the red sea. Science 229 (4708): 49–51. DOI: 10.1126/science.229.4708.49.

Flood BE, Mußmann M, Bailey JV, et al. (2016) Single‐cell Sequencing of Thiomargarita reveals genomic flexibility for adaptation to dynamic redox conditions. Frontiers in Microbiology 7 (June): 1–16. DOI: 10.3389/fmicb.2016.00964.

Fuerst JA (2006) Membrane‐bounded nucleoids and pirellulosomes of Planctomycetes. In: Shively JM (ed.) Complex Intracellular Structures in Prokaryotes. Microbiology Monographs, vol. 2. Springer: Berlin, Heidelberg.

Gallet R, Violle C, Fromin N, et al. (2017) The evolution of bacterial cell size: the internal diffusion‐constraint hypothesis. The ISME Journal 11 (7): 1559–1568. DOI: 10.1038/ismej.2017.35.

van Gemerden H (1974) Coexistence of organisms competing for the same substrate: an example among the purple sulfur bacteria. Microbial Ecology 1 (1): 104–119. DOI: 10.1007/BF02512382.

Graber JR and Breznak JA (2004) Physiology and nutrition of treponema primitia, an H2/CO2‐acetogenic Spirochete from termite hindguts. Applied and Environmental Microbiology 70 (3): 1307–1314. DOI: 10.1128/AEM.70.3.1307‐1314.2004.

Graber JR, Leadbetter JR and Breznak JA (2004) Description of Treponema azotonutricium sp. nov. and Treponema primitia sp. nov., the first spirochetes isolated from termite guts. Applied and Environmental Microbiology 70 (3): 1315–1320. DOI: 10.1128/AEM.70.3.1315‐1320.2004.

Guerrero R, Pedros‐Alio C, Esteve I, et al. (2006) Predatory prokaryotes: Predation and primary consumption evolved in bacteria. Proceedings of the National Academy of Sciences 83 (7). DOI: 2138–2142 DOI: 10.1073/pnas.83.7.2138.

Han C, Markowitz V, Huntemann M, et al. (2013) Genome sequence of the thermophilic fresh‐water bacterium Spirochaeta caldaria type strain (H1T), reclassification of Spirochaeta caldaria, Spirochaeta stenostrepta, and Spirochaeta zuelzerae in the genus Treponema as Treponema caldaria comb. nov., Trepon. Standards in Genomic Sciences 8 (1): 88–105. DOI: 10.4056/sigs.3096473.

Hubalek V, Wu X, Eiler A, et al. (2016) Connectivity to the surface determines diversity patterns in subsurface aquifers of the Fennoscandian shield. The ISME Journal 10 (10): 2447–2458. DOI: 10.1038/ismej.2016.36.

Hylemon PB, Wells JS, Bowdre JH, Macadoo TO and Krieg NR (2009) Designation of Spirillum volutans Ehrenberg 1832 as type species of the genus Spirillum Ehrenberg 1832 and Designation of the neotype strain of S. volutans: Request for an Opinion. International Journal of Systematic Bacteriology 23 (23): 20–27. DOI: 10.1099/00207713‐23‐1‐20.

Iida T, Ohkuma M, Ohtoko K and Kudo T (2000) Symbiotic spirochetes in the termite hindgut: Phylogenetic identification of ectosymbiotic spirochetes of oxymonad protists. FEMS Microbiology Ecology 34 (34): 17–26. DOI: 10.1016/S0168‐6496(00)00070‐2.

Imhoff JF (2015) Thiospirillum. In: Bergey's Manual of Systematics of Archaea and Bacteria, pp 1–3. John Wiley & Sons, Ltd: Chichester, UK. DOI: 10.1002/9781118960608.gbm01126.

Ionescu D, Bizic‐Ionescu M, De Maio N, Cypionka H and Grossart H‐P (2017) Community‐like genome in single cells of the sulfur bacterium Achromatium oxaliferum. Nature Communications 8 (1). DOI: 10.1038/s41467‐017‐00342‐9.

Jørgensen BB and Gallardo VA (1999) Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles. FEMS Microbiology Ecology 28 (4). DOI: 301–313 DOI: 10.1016/S0168‐6496(98)00122‐6.

Kojima H, Ogura Y, Yamamoto N, et al. (2015) Ecophysiology of Thioploca ingrica as revealed by the complete genome sequence supplemented with proteomic evidence. ISME Journal 9 (5): 1166–1176. DOI: 10.1038/ismej.2014.209.

Krauss M and Haucke V (2005) Protein and membrane transport in eukaryotic cells. In: Encyclopedic Reference of Genomics and Proteomics in Molecular Medicine, pp 1473–1477. Springer: Berlin Heidelberg. DOI: 10.1007/3‐540‐29623‐9_4150.

Leschine S and Paster BJ (2015) Spirochaeta. Bergey's Manual of Systematics of Archaea and Bacteria 180: 1–18. DOI: 10.1002/9781118960608.gbm01248.

Li C, Motaleb MA, Sal M, Goldstein SF and Charon NW (2000) Spirochete periplasmic flagella and motility. Journal of Molecular Microbiology and Biotechnology 2 (4): 345–354 Available at: http://www.ncbi.nlm.nih.gov/pubmed/11075905.

Luedin SM, Liechti N, Cox RP, et al. (2019) Draft genome sequence of Chromatium okenii isolated from the stratified alpine Lake Cadagno. Scientific Reports 9 (1). DOI: 1936 DOI: 10.1038/s41598‐018‐38202‐1.

Margulis L and Hinkle G (2013) Large Symbiotic Spirochetes: Clevelandina, Cristispira, Diplocalyx, Hollandina, and Pillotina. In: The Prokaryotes, pp 3965–3978. DOI: 10.1007/978‐1‐4757‐2191‐1_59.

Mendell JE, Clements KD, Choat JH and Angert ER (2008) Extreme polyploidy in a large bacterium. Proceedings of the National Academy of Sciences 105 (18): 6730–6734. DOI: 10.1073/pnas.0707522105.

Meysman FJR (2018) Cable bacteria take a new breath using long‐distance electricity. Trends in Microbiology 26 (5): 411–422. DOI: 10.1016/j.tim.2017.10.011.

Miyake S, Ngugi DK and Stingl U (2016) Phylogenetic diversity, distribution, and cophylogeny of giant bacteria (Epulopiscium) with their Surgeonfish Hosts in the Red Sea. Frontiers in Microbiology 7: 285. DOI: 10.3389/fmicb.2016.00285.

Mußmann M, Hu FZ, Richter M, et al. (2007) Insights into the genome of large sulfur bacteria revealed by analysis of single filaments (NA Moran, ed.). PLoS Biology 5 (9): e230. DOI: 10.1371/journal.pbio.0050230.

Ngugi DK, Miyake S, Cahill M, et al. (2017) Genomic diversification of giant enteric symbionts reflects host dietary lifestyles. Proceedings of the National Academy of Sciences of the United States of America 114 (36): E7592–E7601. DOI: 10.1073/pnas.1703070114.

Paster BJ (2011) Phylum XV. Spirochaetes. In: Garrity GM and Holt JG (eds) Bergey's Manual® of Systematic Bacteriology, pp 471–566. DOI: 10.1007/978‐0‐387‐68572‐4_4.

Puente‐Sánchez F, Arce‐Rodríguez A, Oggerin M, et al. (2018) Viable Cyanobacteria in the deep continental subsurface. Proceedings of the National Academy of Sciences of the United States of America 115 (42): 10702–10707. DOI: 10.1073/pnas.1808176115.

Salman V, Amann R, Girnth A‐C, et al. (2011) A single‐cell sequencing approach to the classification of large, vacuolated sulfur bacteria. Systematic and Applied Microbiology 34 (4): 243–259. DOI: 10.1016/J.SYAPM.2011.02.001.

Salman V, Amann R, Shub DA and Schulz‐Vogt HN (2012) Multiple self‐splicing introns in the 16S rRNA genes of giant sulfur bacteria. Proceedings of the National Academy of Sciences 109 (11): 4203–4208. DOI: 10.1073/pnas.1120192109.

Salman V, Yang T, Berben T, et al. (2015) Calcite‐accumulating large sulfur bacteria of the genus Achromatium in Sippewissett Salt Marsh. ISME Journal 9 (11): 2503–2514. DOI: 10.1038/ismej.2015.62.

Schlegel HG and Pfennig N (1960) Die Anreicherungskultur einiger Schwefelpurpurbakterien. Archiv für Mikrobiologie 38 (1): 1–39. DOI: 10.1007/BF00408405.

Schulz HN, Brinkhoff T, Ferdelman TG, et al. (1999) Dense populations of a giant sulfur bacterium in Namibian shelf sediments. Science 284 (5413): 493–495. DOI: 10.1126/SCIENCE.284.5413.493.

Schulz HN and Jørgensen BB (2002) Big bacteria. Annual Review of Microbiology 55 (1): 105–137. DOI: 10.1146/annurev.micro.55.1.105.

Schulz HN (2006) The Genus Thiomargarita. In: The Prokaryotes, pp 1156–1163. Springer: New York. DOI: 10.1007/0‐387‐30746‐X_47.

Shafrir Y, ben‐Avraham D and Forgacs G (2000) Trafficking and signaling through the cytoskeleton: a specific mechanism. Journal of Cell Science 113 (15).

Teske A and Salman V (2014) The family Beggiatoaceae. In: The Prokaryotes, pp 93–134. Springer: Berlin, Heidelberg. DOI: 10.1007/978‐3‐642‐38922‐1_290.

Wayne LG (2009) Actions of the Judicial Commission of the International Committee on Systematic Bacteriology on requests for opinions published between January 1985 and July 1993. International Journal of Systematic Bacteriology 44 (1): 177–178. DOI: 10.1099/00207713‐44‐1‐177.

Winkel M, Salman‐Carvalho V, Woyke T, et al. (2016) Single‐cell sequencing of Thiomargarita reveals genomic flexibility for adaptation to dynamic redox conditions. Frontiers in Microbiology 7: 964. DOI: 10.3389/fmicb.2016.00964.

Witty M (2009) Spirochetes in the Context of their Environment and Other Microbes. Available at: http://www.asmscience.org/content/education/imagegallery/image.3199 (Accessed 28 March 2019).

Further Reading

Garcia‐Pichel F (1989) Rapid bacterial swimming measured in swarming cells of Thiovulum majus. Journal of Bacteriology 171 (6): 3560–3563.

Garcia‐Pichel F (2000) Cyanobacteria. In: Lederberg J (ed.) Encyclopedia of Microbiology, 2nd edn. Academic Press: San Diego, CA.

Ngugi DK, Miyake S, Cahill M, et al. (2017) Genomic diversification of giant enteric symbionts reflects host dietary lifestyles. Proceedings of the National Academy of Sciences of the United States of America 114 (36): E7592–E7601.

Sand‐Jensen K (2014) Ecophysiology of gelatinous Nostoc colonies: unprecedented slow growth and survival in resource‐poor and harsh environments. Annals of Botany 114 (1): 17–33.

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Ionescu, Danny, and Bizic, Mina(Jul 2019) Giant Bacteria. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0020371.pub2]