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Ion regulation at gills precedes gas exchange and the origin of vertebrates - Nature.com

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Abstract

Gas exchange and ion regulation at gills have key roles in the evolution of vertebrates1,2,3,4. Gills are hypothesized to have first acquired these important homeostatic functions from the skin in stem vertebrates, facilitating the evolution of larger, more-active modes of life2,3,5. However, this hypothesis lacks functional support in relevant taxa. Here we characterize the function of gills and skin in a vertebrate (lamprey ammocoete; Entosphenus tridentatus), a cephalochordate (amphioxus; Branchiostoma floridae) and a hemichordate (acorn worm; Saccoglossus kowalevskii) with the presumed burrowing, filter-feeding traits of vertebrate ancestors6,7,8,9. We provide functional support for a vertebrate origin of gas exchange at the gills with increasing body size and activity, as direct measurements in vivo reveal that gills are the dominant site of gas exchange only in ammocoetes, and only with increasing body size or challenges to oxygen supply and demand. Conversely, gills of all three taxa are implicated in ion regulation. Ammocoete gills are responsible for all ion flux at all body sizes, whereas molecular markers for ion regulation are higher in the gills than in the skin of amphioxus and acorn worms. This suggests that ion regulation at gills has an earlier origin than gas exchange that is unrelated to vertebrate size and activity—perhaps at the very inception of pharyngeal pores in stem deuterostomes.

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Fig. 1: Gill contributions to gas exchange and ion regulation in ammocoetes (E. tridentatus).
Fig. 2: Gas exchange in whole and halved acorn worms (S. kowalevskii).
Fig. 3: Ionocyte marker activity and expression in amphioxus (B. floridae) and acorn worms (S. kowalevskii).
Fig. 4: Putative ionocytes in the pharyngeal gill bars of amphioxus (B. floridae) and acorn worms (S. kowalevskii).

Data availability

All data generated and analysed by this study are publicly accessible (https://doi.org/10.5281/zenodo.7022487). NCBI accession numbers for species and sequences used in gene expression are as follows: txid7739 (M97571.1, XM_002605269.1, XM_002594257.1, XM_002604676.1, XM_002608239.1 and XM_002597600.1) and txid10224 (L28054.1, XM_002736626.2, XM_006814054.1, NM_001184809.1, XM_002734648.1 and XM_002741628.2). NCBI accession numbers for species and sequences used in protein alignments are as follows: txid7739 (XP_002605315.1, XP_002594302.1, XP_002608285.1 and XP_002597646.1), txid10224 (XP_002736672.2, XP_006814117.1, XP_002734694.1 and XP_002741674.2), txid7955 (NP_001161738.1, NP_001032314.1, NP_001289693.1, NP_001032198.1, XP_696967.3, XP_009296364.1, NP_001315073.1, NP_001075158.1, NP_954685.2, NP_001107879.2, NP_001159683.1, NP_001104671.1, XP_009295179.1, NP_957107.1, NP_001017571.2, XP_694982.3, NP_571142.1, NP_571577.1, NP_859424.1, NP_957278.1, NP_944598.2, NP_944599.2, NP_944600.1, NP_001070174.2, NP_956196.1, NP_001030156.1, XP_021335149.1, XP_021334721.1, NP_001106952.1, NP_001107567.1, XP_00929331.1, NP_001106943.1, NP_001091726.2, NP_001025248.2 and NP_001008586.1) and txid9606 (NP_000333.1, NP_001186621.1, NP_005061.3, NP_001076002.1, NP_001209.1, NP_940986.1, NP_036245.1, NP_000058.1, NP_000708.1, NP_001354154.1, NP_001257431.1, NP_001014435.1, NP_001308767.1, NP_001207.2, NP_005240.3, NP_003914.1, NP_005241.1, NP_036320.2, NP_658982.1, NP_997309.2, NP_001129121.1, NP_001445.2, NP_001032242.1, NP_001091954.1, NP_597812.1, NP_001171486.1, NP_003038, NP_003039, NP_004165, NP_001310902.1, NP_001171122.1, NP_001244220.1 and NP_001247420.1). Relevant accession numbers are also provided in the figure source data files. A putative DNA-binding domain was identified in NP_005241.1 using the PROSITE database (https://prosite.expasy.org). Source data are provided with this paper.

References

  1. Evans, D. Gill Na+/H+ and Cl/HCO3 exchange systems evolved before the vertebrates entered fresh water. J. Exp. Biol. 113, 465–469 (1984).

    Article  CAS  PubMed  Google Scholar 

  2. Gans, C. & Northcutt, R. G. Neural crest and the origin of vertebrates: a new head. Science 220, 268–273 (1983).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Northcutt, R. G. The new head hypothesis revisited. J. Exp. Zoolog. B 304, 274–297 (2005).

    Article  Google Scholar 

  4. Halstead, L. B. & Lawson, J. D. The vertebrate invasion of fresh water. Philos. Trans. R. Soc. B 309, 243–258 (1985).

    ADS  Google Scholar 

  5. Brauner, C. J. & Rombough, P. J. Ontogeny and paleophysiology of the gill: new insights from larval and air-breathing fish. Respir. Physiol. Neurobiol. 184, 293–300 (2012).

    Article  PubMed  Google Scholar 

  6. Purnell, M. A. Feeding in extinct jawless heterostracan fishes and testing scenarios of early vertebrate evolution. Proc. R. Soc. B 269, 83–88 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  7. Simakov, O. et al. Hemichordate genomes and deuterostome origins. Nature 527, 459–465 (2015).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Green, S. A., Simoes-Costa, M. & Bronner, M. E. Evolution of vertebrates as viewed from the crest. Nature 520, 474–482 (2015).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Lowe, C. J., Clarke, D. N., Medeiros, D. M., Rokhsar, D. S. & Gerhart, J. The deuterostome context of chordate origins. Nature 520, 456–465 (2015).

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Ronco, F. et al. Drivers and dynamics of a massive adaptive radiation in cichlid fishes. Nature 589, 76–81 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  11. Gillis, J. A. & Tidswell, O. R. A. The origin of vertebrate gills. Curr. Biol. 27, 729–732 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Green, S. A. & Bronner, M. E. The lamprey: a jawless vertebrate model system for examining origin of the neural crest and other vertebrate traits. Differentiation 87, 44–51 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Mongera, A. et al. Genetic lineage labeling in zebrafish uncovers novel neural crest contributions to the head, including gill pillar cells. Development 140, 916–925 (2013).

    Article  CAS  PubMed  Google Scholar 

  14. Morris, S. C. & Caron, J.-B. A primitive fish from the Cambrian of North America. Nature 512, 419–422 (2014).

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Shu, D.-G. et al. Lower Cambrian vertebrates from south China. Nature 402, 42–46 (1999).

    Article  ADS  CAS  Google Scholar 

  16. Xian-guang, H., Aldridge, R. J., Siveter, D. J., Siveter, D. J. & Xiang-hong, F. New evidence on the anatomy and phylogeny of the earliest vertebrates. Proc. R. Soc. B 269, 1865–1869 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Fu, C., Wilson, J. M., Rombough, P. J. & Brauner, C. J. Ions first: Na+ uptake shifts from the skin to the gills before O2 uptake in developing rainbow trout, Oncorhynchus mykiss. Proc. R. Soc. B 277, 1553–1560 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rombough, P. The functional ontogeny of the teleost gill: which comes first, gas or ion exchange? Comp. Biochem. Physiol. A 148, 732–742 (2007).

    Article  Google Scholar 

  19. Gillis, J. A., Fritzenwanker, J. H. & Lowe, C. J. A stem-deuterostome origin of the vertebrate pharyngeal transcriptional network. Proc. R. Soc. B 279, 237–246 (2012).

    Article  PubMed  Google Scholar 

  20. Miyashita, T., Gess, R. W., Tietjen, K. & Coates, M. I. Non-ammocoete larvae of Palaeozoic stem lampreys. Nature 591, 408–412 (2021).

    Article  ADS  CAS  PubMed  Google Scholar 

  21. Dawson, H. A., Quintella, B. R., Almeida, P. R., Treble, A. J. & Jolley, J. C. in Lampreys: Biology, Conservation and Control (ed. Docker, M. F.) 75–137 (Springer, 2015).

  22. Wilkie, M. P., Bradshaw, P. G., Joanis, V., Claude, J. F. & Swindell, S. L. Rapid metabolic recovery following vigorous exercise in burrow‐dwelling larval sea lampreys (Petromyzon marinus). Physiol. Biochem. Zool. 74, 261–272 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. Wells, P. & Pinder, A. The respiratory development of Atlantic salmon. I. Morphometry of gills, yolk sac and body surface. J. Exp. Biol. 199, 2725–2736 (1996).

    Article  CAS  PubMed  Google Scholar 

  24. Perry, S. F. & Wood, C. M. Kinetics of branchial calcium uptake in the rainbow trout: effects of acclimation to various external calcium levels. J. Exp. Biol. 116, 411–433 (1985).

    Article  Google Scholar 

  25. Hwang, P.-P. & Lin, L. Y. in The Physiology of Fishes 4th edn (eds Evans, D. H., Claiborne, J. B. & Currie, S.) 205–234 (CRC Press, 2013).

  26. Blair, S. D., Wilkie, M. P. & Edwards, S. L. Rh glycoprotein immunoreactivity in the skin and its role in extrabranchial ammonia excretion by the sea lamprey (Petromyzon marinus) in freshwater. Can. J. Zool. 95, 95–105 (2017).

    Article  CAS  Google Scholar 

  27. Tweedell, K. S. Regeneration of the enteropneust, Saccoglossus kowalevskii. Biol. Bull. 120, 118–127 (1961).

    Article  Google Scholar 

  28. Schulte, P. M. The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment. J. Exp. Biol. 218, 1856–1866 (2015).

    Article  PubMed  Google Scholar 

  29. Barrington, E. J. The Biology of Hemichordata and Protochordata (Oliver and Boyd, 1965).

  30. Richards, J. G. Physiological, behavioral and biochemical adaptations of intertidal fishes to hypoxia. J. Exp. Biol. 214, 191–199 (2011).

    Article  PubMed  Google Scholar 

  31. Miyamoto, N. & Wada, H. in Oxford Research Encyclopedia of Neuroscience https://doi.org/10.1093/acrefore/9780190264086.013.204 (Oxford Univ. Press, 2018).

  32. Schmitz, A., Gemmel, M. & Perry, S. F. Morphometric partitioning of respiratory surfaces in amphioxus (Branchiostoma lanceolatum Pallas). J. Exp. Biol. 203, 3381–3390 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Wells, P. & Pinder, A. The respiratory development of Atlantic salmon. II. Partitioning of oxygen uptake among gills, yolk sac and body surfaces. J. Exp. Biol. 199, 2737–2744 (1996).

    Article  CAS  PubMed  Google Scholar 

  34. Hsiao, C.-D. et al. A positive regulatory loop between foxi3a and foxi3b is essential for specification and differentiation of zebrafish epidermal ionocytes. PLoS ONE 2, e302 (2007).

  35. Montoro, D. T. et al. A revised airway epithelial hierarchy includes CFTR-expressing ionocytes. Nature 560, 319–324 (2018).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  36. Quigley, I. K., Stubbs, J. L. & Kintner, C. Specification of ion transport cells in the Xenopus larval skin. Development 138, 705–714 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Richards, J. G., Semple, J. W., Bystriansky, J. S. & Schulte, P. M. Na+/K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J. Exp. Biol. 206, 4475–4486 (2003).

    Article  CAS  PubMed  Google Scholar 

  38. Tresguerres, M., Katoh, F., Fenton, H., Jasinska, E. & Goss, G. G. Regulation of branchial V-H+-ATPase, Na+/K+-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J. Exp. Biol. 208, 345–354 (2005).

    Article  CAS  PubMed  Google Scholar 

  39. Cuoghi, I., Lazzaretti, C., Mandrioli, M., Mola, L. & Pederzoli, A. Immunohistochemical analysis of the distribution of molecules involved in ionic and pH regulation in the lancelet Branchiostoma floridae (Hubbs, 1922). Acta Histochem. 120, 33–40 (2018).

    Article  CAS  PubMed  Google Scholar 

  40. Li, M., Jiang, C., Zhang, Y. & Zhang, S. Activities of amphioxus GH-like protein in osmoregulation: insight into origin of vertebrate GH family. Int. J. Endocrinol. 2017, 9538685 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Sackville, M. A. et al. Water pH limits extracellular but not intracellular pH compensation in the CO2-tolerant freshwater fish Pangasianodon hypophthalmus. J. Exp. Biol. 221, jeb190413 (2018).

    Article  PubMed  Google Scholar 

  42. Stone, J. R. & Hall, B. K. Latent homologues for the neural crest as an evolutionary novelty. Evol. Dev. 6, 123–129 (2004).

    Article  PubMed  Google Scholar 

  43. Stumpp, M. & Hu, M. Y. in Acid–Base Balance and Nitrogen Excretion in Invertebrates (eds Weihrauch, D. & O’Donnell, M.) 261–273 (Springer, 2017).

  44. Gonzalez, P. & Cameron, C. B. The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures. Biol. J. Linn. Soc. 98, 898–906 (2009).

    Article  Google Scholar 

  45. Blewett, T. A. & Goss, G. G. A novel pathway of nutrient absorption in crustaceans: branchial amino acid uptake in the green shore crab (Carcinus maenas). Proc. R. Soc. B 284, 20171298 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Quinton, P. M. Role of epithelial HCO3 transport in mucin secretion: lessons from cystic fibrosis. Am. J. Physiol. Cell Physiol. 299, C1222–C1233 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Pardos, F. & Benito, J. Estudio histológico de lar faringe de Glossobalanus minutus (Enteropneusta, Ptychoderidae). Bol. R. Soc. Espanõla Hist. Nat. 80, 101–118 (1982).

    Google Scholar 

  48. Ruppert, E. E. in Microscopic Anatomy of Invertebrates Vol. 15 (eds Harrison, F. W. & Ruppert, E. E.) 349–504 (John Wiley & Sons, 1997).

  49. Mallatt, J. The suspension feeding mechanism of the larval lamprey Petromyzon marinus. J. Zool. 194, 103–142 (1981).

    Article  Google Scholar 

  50. Water Quality Control Annual Report http://www.metrovancouver.org/services/parks/ParksPublications/2018WaterQualityMonitoringReport.pdf (Metro Vancouver, 2018).

  51. Lowe, C. J., Tagawa, K., Humphreys, T., Kirschner, M. & Gerhart, J. in Methods in Cell Biology Vol. 74 (eds Ettensohn, C. A., Wray, G. A. & Wessel, G. M.) 171–194 (Elsevier, 2004).

  52. Boutilier, R. G., Heming, T. A. & Iwama, G. K. in Fish Physiology Vol. 10 (eds Hoar, W.S. & Randall, D. J.) 403–430 (Elsevier, 1984).

  53. Verdouw, H., Van Echteld, C. J. A. & Dekkers, E. M. J. Ammonia determination based on indophenol formation with sodium salicylate. Water Res. 12, 399–402 (1978).

    Article  CAS  Google Scholar 

  54. Lee, D. J., Gutbrod, M., Ferreras, F. M. & Matthews, P. G. D. Changes in hemolymph total CO2 content during the water-to-air respiratory transition of amphibiotic dragonflies. J. Exp. Biol. 221, jeb181438 (2018).

    Article  PubMed  Google Scholar 

  55. Brauner, C. J. & Wood, C. M. Ionoregulatory development and the effect of chronic silver exposure on growth, survival, and sublethal indicators of toxicity in early life stages of rainbow trout (Oncorhynchus mykiss). J. Comp. Physiol. B 172, 153–162 (2002).

    Article  CAS  PubMed  Google Scholar 

  56. Zimmer, A. M., Brix, K. V. & Wood, C. M. Mechanisms of Ca2+ uptake in freshwater and seawater-acclimated killifish, Fundulus heteroclitus, and their response to acute salinity transfer. J. Comp. Physiol. B 189, 47–60 (2019).

    Article  CAS  PubMed  Google Scholar 

  57. Zimmer, A. M., Wright, P. A. & Wood, C. M. What is the primary function of the early teleost gill? Evidence for Na+/NH4+ exchange in developing rainbow trout (Oncorhynchus mykiss). Proc. R. Soc. B 281, 20141422 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Sackville, M., Wilson, J. M., Farrell, A. P. & Brauner, C. J. Water balance trumps ion balance for early marine survival of juvenile pink salmon (Oncorhynchus gorbuscha). J. Comp. Physiol. B 182, 781–792 (2012).

    Article  CAS  PubMed  Google Scholar 

  59. McCormick, S. D. Methods for nonlethal gill biopsy and measurement of Na+, K+-ATPase activity. Can. J. Fish. Aquat. Sci. 50, 656–658 (1993).

    Article  CAS  Google Scholar 

  60. Ward, N. & Moreno-Hagelsieb, G. Quickly finding orthologs as reciprocal best hits with BLAT, LAST, and UBLAST: how much do we miss? PLoS ONE 9, e101850 (2014).

  61. Gibbons, T. C., Metzger, D. C. H., Healy, T. M. & Schulte, P. M. Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats. Mol. Ecol. 26, 2711–2725 (2017).

    Article  CAS  PubMed  Google Scholar 

  62. Hirschberger, C. & Gillis, J. A. The pseudobranch of jawed vertebrates is a mandibular arch-derived gill. Development 149, dev200184 (2022).

  63. Uchida, K., Kaneko, T., Miyazaki, H., Hasegawa, S. & Hirano, T. Excellent salinity tolerance of Mozambique tilapia (Oreochromis mossambicus): elevated chloride cell activity in the branchial and opercular epithelia of the fish adapted to concentrated seawater. Zoolog. Sci. 17, 149–160 (2000).

    Article  Google Scholar 

  64. Choi, H. M. T. et al. Third-generation in situ hybridization chain reaction: multiplexed, quantitative, sensitive, versatile, robust. Development 145, dev165753 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Criswell, K. E. & Gillis, J. A. Resegmentation is an ancestral feature of the gnathostome vertebral skeleton. eLife 9, e51696 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Witten, P. E. & Hall, B. K. Seasonal changes in the lower jaw skeleton in male Atlantic salmon (Salmo salar L.): remodelling and regression of the kype after spawning. J. Anat. 203, 435–450 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank P. J. Rombough for discussion that helped inspire this work. This study was funded in part by Natural Sciences and Engineering Council of Canada Discovery Grants to C.J.B. (2018-04172) and C.B.C. (1283784), and a Royal Society University Research Fellowship (UF130182, URF\R\191007) and Royal Society Research Fellows Enhancement Award (RGF/EA/180087) to J.A.G. M.A.S. was supported by an NSERC CGS-D scholarship.

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M.A.S., C.J.B. and C.B.C. conceived the study. M.A.S. performed all experiments and data analyses and wrote the manuscript. J.A.G. oversaw all microscopy. All authors provided manuscript edits and comments and approved the final version.

Corresponding author

Correspondence to Michael A. Sackville.

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Nature thanks Dorit Hockman, Christopher Lowe and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Cutaneous diffusive capacity of ammocoetes (E. tridentatus).

Mass-specific surface area (a; n = 15) and epidermal thickness (b; n = 16) measured in different subsets of ammocoetes. Diffusive capacity of the skin (c) calculated from allometric curves fitted to epidermal thickness (a) and mass-specific surface area (b). All data expressed as a function of wet mass (g).

Source data

Extended Data Fig. 2 Gill contributions to CO2 and calcium flux in ammocoetes (E. tridentatus).

Gill contributions (a) and whole-body flux rates (b, c) for CO2 excretion (white), oxygen uptake (grey) and calcium uptake (green) in normoxia at 20 °C. Individual data points plotted as a function of wet mass (g), n = 8 for all groups except n = 7 for gill contributions to calcium uptake

Source data

Extended Data Fig. 3 Whole-body rates of gas and ion flux in ammocoetes (E. tridentatus).

Rates of oxygen uptake (a; n = 40), ammonia excretion (b; n = 36) and sodium uptake (c; n = 21) in normoxia at 10 °C, 26 °C (grey; oxygen only, n = 26) or hypoxia at 20 °C (white; oxygen only, n = 22). Individual data points plotted as a function of wet mass (g)

Source data

Extended Data Fig. 4 ATPase activities in acorn worms (S. kowalevskii), amphioxus (B. floridae) and ammocoetes (E. tridentatus).

Na+/K+-ATPase (ac; NKA) and V-H+-ATPase (d,e; VHA) activities in multiple tissues of S. kowalevskii (a,d), B. floridae (b,e) and E. tridentatus (c). Data presented as means±sd with individuals superimposed (n = 10 for all tissues except n = 9 for proboscis and hepatic caecum). One-way ANOVA with Tukey’s test (a,b,d) or Kruskal-Wallis with Dunn’s test (c,e), P < 0.05. Letters indicate significant differences between tissues. P < 0.0001 (ac,e), P = 0.6203 (d).

Source data

Extended Data Fig. 5 Gene expression for ionocyte markers in amphioxus (B. floridae).

Anion exchanger (a; AE, P < 0.0001), sodium–proton exchanger (b; NHE, P < 0.0001), carbonic anhydrase (c; CA, P = 0.0004) and forkhead box protein I (d; FoxI, P < 0.0001) expression in skin, gill, hepatic caecum and muscle of B. floridae. Expression is relative to geometric mean of EF1A and 18S. Data presented as means±sd with individuals superimposed (n = 10). One-way ANOVA with Tukey’s test, P < 0.05. Letters indicate significant differences between tissues

Source data

Extended Data Fig. 6 Gene expression for ionocyte markers in acorn worms (S. kowalevskii).

Anion exchanger (a; AE, P = 0.0163), sodium-proton exchanger (b; NHE, P < 0.0001), carbonic anhydrase (c; CA, P = 0.0431) and forkhead box protein I (d; FoxI, P < 0.0001) expression in skin, gill, intestine and proboscis of S. kowalevskii. Expression is relative to geometric mean of EF1A and 18S. Data presented as means±sd with individuals superimposed (n = 10). Letters indicate significant differences between tissues. One-way ANOVA with Tukey’s test (b,d) or Kruskal-Wallis with Dunn’s test (a,c), P < 0.05

Source data

Extended Data Fig. 7 Origins of gill function.

Our findings support a novel stem chordate or deuterostome origin for ion regulation at gills (pink), perhaps near the inception of pharyngeal gill pores and their role in filter-feeding (black). A vertebrate origin for gas exchange at gills (blue) with increasing body size and activity is also supported by this work, and consistent with fossil and developmental studies (references in text). Data not collected for clades in grey.

Extended Data Fig. 8 Acidic mucins in the foxI+ domains of the pharyngeal gill bars in B. floridae.

Positive staining for Alcian blue shows acidic mucins in the foxI+ domains of the pharyngeal gill bars in B. floridae (outlined section). Counterstained with Nuclear Fast Red, scale bar = 50 μm. This experiment was repeated independently three times with similar results.

Extended Data Table 1 NCBI accession numbers for target proteins and genes in Danio rerio and their reciprocal best BLAST hits in Branchiostoma floridae and Saccoglossus kowalevskii
Extended Data Table 2 Primer sequences for qRT–PCR in Branchiostoma floridae (bf) and Saccoglossus kowalevskii (sk)

Supplementary information

Supplementary Information

This file contains Supplementary Methods; Supplementary Data Tables 1-2; Supplementary Figures 1–8 and Supplementary References.

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Sackville, M.A., Cameron, C.B., Gillis, J.A. et al. Ion regulation at gills precedes gas exchange and the origin of vertebrates. Nature (2022). https://ift.tt/zghvWqU

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