Sudhakar SIVASUBRAMANIAM, Elaiya Raja SUBRAMANIAN, * Dinesh Kumar SUDALAIMANI1, Johnson Retnaraj Samuel CHRISTYRAJ SELVAN, Kalidas RAMAMOORTHY, Nino DAISY GOPI, Jackson Durairaj SELVAN CHRISTYRAJ, Kasimani RENGANATHAN, Sundar KRISHNAN

Studies on organogenesis during regeneration in the earthworm, Eudrilus eugeniae, in support of symbiotic association with Bacillus endophyticus

Organogenesis and animal adaptation upon loss of body parts are crucial events in regeneration of all traits, and both are uncovered areas in biology. The organogenesis of the mouth and anus during regeneration was studied in Eudrilus eugeniae. It was found that the earthworm regenerates a functional mouth and anus in six days. During the course of organogenesis, the earthworm adopts unique starvation behavior for 5 days, and the starvation triggers the gut microflora of E. eugeniae to produce riboflavin. One of the efficient riboflavin-producing bacteria, Bacillus endophyticus, confirmed through 16S rRNA sequencing, has been isolated from its gut. The symbiotic association provides shelter and nutrition to the bacterium and the earthworm in return gets riboflavin to maintain homeostasis during the starvation period of early regeneration.

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Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014). The placenta harbors a unique microbiome. Sci Transl Med 6: 237ra65.
Barile M, Brizio C, Virgilio C, Delfine S, Quagliariello E, Passarella S (1997). Flavin adenine dinucleotide and flavin mononucleotide metabolism in rat liver. Eur J Biochem 249: 777-785.
Bayliss PE, Bellavance KL, Whitehead GG, Abrams JM, Aegerter S, Robbins HS, Cowan DB, Keating MT, OReilly T, Wood JM (2006). Chemical modulation of receptor signaling inhibits regenerative angiogenesis in adult zebrafish. Nat Chem Biol 2: 265-273.
Bely AE, Nyberg KG (2010). Evolution of animal regeneration: reemergence of a field. Trends Ecol Evol 25: 161-170.
Broun M, Gee L, Reinhardt B, Bode HR (2005). Formation of the head organizer in hydra involves the canonical Wnt pathway. Development 132: 2907-2916.
Cappon G, Fleeman T, Chapin R, Hurtt M (2005). Effects of feed restriction during organogenesis on embryo‐fetal development in rabbit. Birth Defects Res B 74: 424-430.
Cho SJ, Koh KS, Lee E, Park SC (2009). Differential expression of three labial genes during earthworm head regeneration. Biosci Biotechnol Biochem 73: 2609-2614.
Depeint F, Bruce WR, Shangari N, Mehta R, OBrien PJ (2006). Mitochondrial function and toxicity: role of the B vitamin family on mitochondrial energy metabolism. Chem Biol Interact 163: 94-112.
Ding BS, Nolan DJ, Butler JM, James D, Babazadeh AO, Rosenwaks Z, Mittal V, Kobayashi H, Shido K, Lyden D et al. (2010). Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 468: 310-315.
Drixler TA, Vogten MJ, Ritchie ED, van Vroonhoven TJ, Gebbink MF, Voest EE, Rinkes IHB (2002). Liver regeneration is an angiogenesis-associated phenomenon. Ann Surg 236: 703-712.
Fischer M, Bacher A (2006). Biosynthesis of vitamin B2 in plants. Physiol Plant 126: 304-318.
Funes JM, Quintero M, Henderson S, Martinez D, Qureshi U, Westwood C, Clements MO, Bourboulia D, Pedley RB, Moncada S et al. (2007). Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production. P Natl Acad Sci USA 104: 6223-6228.
Gates G (1949). Regeneration in an earthworm, Eisenia foetida (Savigny) 1826. I. Anterior regeneration. Biol Bull 96: 129-139. Gates GE (1927). Regeneration in a tropical earthworm Perionyx excavatus E. Perr. Biol Bull 53: 351-364.
Goessling W, North TE, Lord AM, Ceol C, Lee S, Weidinger G, Bourque C, Strijbosch R, Haramis AP, Puder M et al. (2008). APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev Biol 320: 161-174.
Gurley KA, Rink JC, Alvarado AS (2008). β-Catenin defines head versus tail identity during planarian regeneration and homeostasis. Science 319: 323-327.
Gurtner GC, Werner S, Barrandon Y, Longaker MT (2008). Wound repair and regeneration. Nature 453: 314-321.
Hill M (1997). Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev 6: S43-S45.
Hobmayer B, Rentzsch F, Kuhn K, Happel CM, von Laue CC, Snyder P, Rothbächer U, Holstein TW (2000). WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 407: 186-189.
Hooper LV, Midtvedt T, Gordon JI (2002). How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22: 283-307.
Hoppel CL, Tandler B (1975). Riboflavin and mouse hepatic cell structure and function. Mitochondrial oxidative metabolism in severe deficiency states. J Nutr 105: 562-570.
Johnson Retnaraj Samuel SC, Elaiya Raja S, Beryl Vedha Y, Edith Arul Jane A, Amutha K, Dinesh SM, Jackson Durairaj SC, Kalidas RM, Tharmaraj V, Pitchumani K (2011). Autofluorescence in BrdU-positive cells and augmentation of regeneration kinetics by riboflavin. Stem Cells Dev 21: 2071-2083.
Kalidas RM, Raja SE, Mydeen SAKNM, Samuel SCJR, Durairaj SCJ, Nino GD, Palanichelvam K, Vaithi A, Sudhakar S (2015). Conserved lamin A protein expression in differentiated cells in the earthworm Eudrilus eugeniae. Cell Biol Int 39: 1036-1043.
Kawasumi A, Sagawa N, Hayashi S, Yokoyama H, Tamura K (2012). Wound healing in mammals and amphibians: toward limb regeneration in mammals. In: Heber-Katz E, Stocum DL, editors. New Perspectives in Regeneration. Berlin, Germany: Springer, pp. 33-49.
Kozlova A, Petukhova O, Pinaev G (2005). The analysis of cellular elements in coelomic fluid during early regeneration of of the starfish Asterias rubens L. Tsitologiia 48: 175-183 (in Russian with abstract in English).
Kumar A, Velloso CP, Imokawa Y, Brockes JP (2000). Plasticity of retrovirus-labelled myotubes in the newt limb regeneration blastema. Dev Biol 218: 125-136.
LeBlanc JG, Milani C, de Giori GS, Sesma F, Van Sinderen D, Ventura M (2013). Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr Opin Biotechnol 24: 160-168.
Maden M, Gale E, Kostetskii I, Zile M (1996). Vitamin A-deficient quail embryos have half a hindbrain and other neural defects. Curr Biol 6: 417-426.
Maden M, Gale E, Zile M (1998). The role of vitamin A in the development of the central nervous system. J Nutr 128: 471S-475S.
Mandal S, Lindgren AG, Srivastava AS, Clark AT, Banerjee U (2011). Mitochondrial function controls proliferation and early differentiation potential of embryonic stem cells. Stem Cells 29: 486-495.
McArdle HJ, Ashworth CJ (1999). Micronutrients in fetal growth and development. Brit Med Bull 55: 499-510.
Moriya A, Fukuwatari T, Shibata K (2013). Excess vitamin intake before starvation does not affect body mass, organ mass, or blood variables but affects urinary excretion of riboflavin in starving rats. Nutr Metab Insights 6: 23.
Nelson DL, Cox M (2013). Lehninger Principles of Biochemistry. San Francisco, CA, USA: W.H. Freeman.
Nicholson JK, Holmes E, Wilson ID (2005). Gut microorganisms, mammalian metabolism and personalized health care. Nat Rev Microbiol 3: 431-438.
Potthoff MJ, Inagaki T, Satapati S, Ding X, He T, Goetz R, Mohammadi M, Finck BN, Mangelsdorf DJ, Kliewer SA et al. (2009). FGF21 induces PGC-1α and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. P Natl Acad Sci USA 106: 10853-10858.
Prabhakar G, Raju D, Satyanarayana M (1993). Bioproduction of riboflavin from molasses and lentils. Bioprocess Eng 8: 247-249.
Quiñones JL, Rosa R, Ruiz DL, García-Arrarás JE (2002). Extracellular matrix remodeling and metalloproteinase involvement during intestine regeneration in the sea cucumber Holothuria glaberrima. Dev Biol 250: 181-197.
Rageh MA, Mendenhall L, Moussad EE, Abbey SE, Mescher AL, Tassava RA (2002). Vasculature in pre‐blastema and nerve‐ dependent blastema stages of regenerating forelimbs of the adult newt, Notophthalmus viridescens. J Exp Zool 292: 255-266.
Rawls JF, Samuel BS, Gordon JI (2004). Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. P Natl Acad Sci USA 101: 4596-4601.
Reddi A, Ho P, Camerini-Davalos R (1979). The role of riboflavin in carbohydrate metabolism. Adv Exp Med Biol 119: 243-250.
Reva ON, Smirnov VV, Pettersson B, Priest FG (2002). Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (Gossypium sp.). Int J Syst Evol Microbiol 52: 101-107.
Sandoval FJ, Zhang Y, Roje S (2008). Flavin nucleotide metabolism in plants monofunctional enzymes synthesize FAD in plastids. J Biol Chem 283: 30890-30900.
Schindler AJ, Baugh LR, Sherwood DR (2014). Identification of late larval stage developmental checkpoints in Caenorhabditis elegans regulated by insulin/IGF and steroid hormone signaling pathways. PLoS Genet 10: e1004426.
Stahmann KP, Kupp C, Feldmann S (1994). Formation and degradation of lipid bodies found in the riboflavin-producing fungus Ashbya gossypii. Appl Microbiol Biotechnol 42: 121- 127.
Sun L, Chen M, Yang H, Wang T, Liu B, Shu C, Gardiner DM (2011). Large scale gene expression profiling during intestine and body wall regeneration in the sea cucumber Apostichopus japonicus. Comp Biochem Phys D 6: 195-205.
Uribe A, Alam M, Midtvedt T, Smedfors B, Theodorsson E (1997). Endogenous prostaglandins and microflora modulate DNA synthesis and neuroendocrine peptides in the rat gastrointestinal tract. Scand J Gastroentero 32: 691-699.
Wagner DE, Wang IE, Reddien PW (2011). Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 332: 811-816.
Xu X, Duan S, Yi F, Ocampo A, Liu GH, Belmonte JCI (2013). Mitochondrial regulation in pluripotent stem cells. Cell Metab 18: 325-332.
Yakovleva TV, Bazhan NM, Makarova EN (1997). Effects of food deprivation in early pregnancy on the development of ovaries and adrenals in female progeny of the water vole (Arvicola terrestris). Comp Biochem Phys C 116: 103-109.
Yoshida‐Noro C, Tochinai S (2010). Stem cell system in asexual and sexual reproduction of Enchytraeus japonensis (Oligochaeta, Annelida). Dev Growth Differ 52: 43-55.
Zhang C, Zhang M, Wang S, Han R, Cao Y, Hua W, Mao Y, Zhang X, Pang X, Wei C et al. (2010). Interactions between gut microbiota, host genetics and diet relevant to development of metabolic syndromes in mice. ISME J 4: 232-241.
Zhang M, Huang B (2012). The multi-differentiation potential of peripheral blood mononuclear cells. Stem Cell Res Ther 3: 1.