Late acquisition of the rTCA carbon fixation pathway by Chlorobi.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
10
02
2023
accepted:
30
06
2023
medline:
8
9
2023
pubmed:
4
8
2023
entrez:
3
8
2023
Statut:
ppublish
Résumé
The reverse tricarboxylic acid (rTCA) cycle is touted as a primordial mode of carbon fixation due to its autocatalytic propensity and oxygen intolerance. Despite this inferred antiquity, however, the earliest rock record affords scant supporting evidence. In fact, based on the chimeric inheritance of rTCA cycle steps within the Chlorobiaceae, even the use of the chemical fossil record of this group is now subject to question. While the 1.64-billion-year-old Barney Creek Formation contains chemical fossils of the earliest known putative Chlorobiaceae-derived carotenoids, interferences from the accompanying hydrocarbon matrix have hitherto precluded the carbon isotope measurements necessary to establish the physiology of the organisms that produced them. Overcoming this obstacle, here we report a suite of compound-specific carbon isotope measurements identifying a cyanobacterially dominated ecosystem featuring heterotrophic bacteria. We demonstrate chlorobactane is
Identifiants
pubmed: 37537385
doi: 10.1038/s41559-023-02147-0
pii: 10.1038/s41559-023-02147-0
doi:
Substances chimiques
Tricarboxylic Acids
0
Carbon Isotopes
0
Carotenoids
36-88-4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1398-1407Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Ward, L. M. & Shih, P. M. The evolution and productivity of carbon fixation pathways in response to changes in oxygen concentration over geological time. Free Radic. Biol. Med. 140, 188–199 (2019).
pubmed: 30790657
doi: 10.1016/j.freeradbiomed.2019.01.049
Hartman, H. Speculations on the origin and evolution of metabolism. J. Mol. Evolution 4, 359–370 (1975).
doi: 10.1007/BF01732537
Wächtershäuser, G. Evolution of the first metabolic cycles. Proc. Natl Acad. Sci. USA 87, 200–204 (1990).
pubmed: 2296579
pmcid: 53229
doi: 10.1073/pnas.87.1.200
Weiss, M. C. et al. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1, 16116 (2016).
pubmed: 27562259
doi: 10.1038/nmicrobiol.2016.116
Kitadai, N., Kameya, M. & Fujishima, K. Origin of the reductive tricarboxylic acid (rTCA) cycle-type CO(
pmcid: 5745552
doi: 10.3390/life7040039
Overmann, J. in Sulfur Metabolism in Phototrophic Organisms (eds Hell, R. et al.) 375–396 (Springer, 2008).
Camacho, A., Walter, X. A., Picazo, A. & Zopfi, J. Photoferrotrophy: remains of an ancient photosynthesis in modern environments. Front. Microbiol. 8, 323 (2017).
pubmed: 28377745
pmcid: 5359306
doi: 10.3389/fmicb.2017.00323
Thompson, K. J., Simister, R. L., Hahn, A. S., Hallam, S. J. & Crowe, S. A. Nutrient acquisition and the metabolic potential of photoferrotrophic Chlorobi. Front. Microbiol. 8, 1212 (2017).
pubmed: 28729857
pmcid: 5498476
doi: 10.3389/fmicb.2017.01212
Fournier, G. P. et al. The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages. Proc. R. Soc. B 288, 20210675 (2021).
pubmed: 34583585
pmcid: 8479356
doi: 10.1098/rspb.2021.0675
Magnabosco, C., Moore, K. R., Wolfe, J. M. & Fournier, G. P. Dating phototrophic microbial lineages with reticulate gene histories. Geobiology 16, 179–189 (2018).
pubmed: 29384268
pmcid: 5873394
doi: 10.1111/gbi.12273
Brocks, J. J. et al. Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 437, 866–870 (2005).
pubmed: 16208367
doi: 10.1038/nature04068
Krügel, H., Krubasik, P., Weber, K., Saluz, H. P. & Sandmann, G. Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1439, 57–64 (1999).
doi: 10.1016/S1388-1981(99)00075-X
Cui, X. et al. Niche expansion for phototrophic sulfur bacteria at the Proterozoic-Phanerozoic transition. Proc. Natl Acad. Sci. USA 117, 17599–17606 (2020).
pubmed: 32647063
pmcid: 7395447
doi: 10.1073/pnas.2006379117
Marin, J., Battistuzzi, F. U., Brown, A. C. & Hedges, S. B. The timetree of prokaryotes: new insights into their evolution and speciation. Mol. Biol. Evol. 34, 437–446 (2016).
Paoletti, M. M. & Fournier, G. P. Chimeric inheritance and crown-group acquisitions of carbon fixation genes within Chlorobiales: origins of autotrophy in Chlorobiales and implication for geological biomarkers. PLoS ONE 17, e0275539 (2022).
pubmed: 36227849
pmcid: 9560492
doi: 10.1371/journal.pone.0275539
Stal, L. J. & Moezelaar, R. Fermentation in cyanobacteria. FEMS Microbiol. Rev. 21, 179–211 (1997).
doi: 10.1016/S0168-6445(97)00056-9
Tang, K.-H. & Blankenship, R. E. Both forward and reverse TCA cycles operate in green sulfur bacteria. J. Biol. Chem. 285, 35848–35854 (2010).
pubmed: 20650900
pmcid: 2975208
doi: 10.1074/jbc.M110.157834
Blair, N., Leu, A., Olsen, J., Kwong, E. & Des Marais, D. Carbon isotopic fractionation in heterotrophic microbial metabolism. Appl. Environ. Microbiol. 50, 996–1001 (1985).
pubmed: 2867741
pmcid: 291782
doi: 10.1128/aem.50.4.996-1001.1985
DeNiro, M. J. & Epstein, S. Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495–506 (1978).
doi: 10.1016/0016-7037(78)90199-0
Badger, M. R. & Bek, E. J. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO
pubmed: 18245799
doi: 10.1093/jxb/erm297
Hanson, T. E. & Tabita, F. R. A ribulose-1, 5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. Proc. Natl Acad. Sci. USA 98, 4397–4402 (2001).
pubmed: 11287671
pmcid: 31846
doi: 10.1073/pnas.081610398
Sirevåg, R., Buchanan, B. B., Berry, J. A. & Troughton, J. H. Mechanisms of CO
pubmed: 402896
doi: 10.1007/BF00446651
Zyakun, A. M., Lunina, O. N., Prusakova, T. S., Pimenov, N. V. & Ivanov, M. V. Fractionation of stable carbon isotopes by photoautotrophically growing anoxygenic purple and green sulfur bacteria. Microbiology 78, 757–768 (2009).
doi: 10.1134/S0026261709060137
Quandt, L., Gottschalk, G., Ziegler, H. & Stichler, W. Isotope discrimination by photosynthetic bacteria. FEMS Microbiol. Lett. 1, 125–128 (1977).
doi: 10.1111/j.1574-6968.1977.tb00596.x
Fulton, J. M., Arthur, M. A., Thomas, B. & Freeman, K. H. Pigment carbon and nitrogen isotopic signatures in euxinic basins. Geobiology 16, 429–445 (2018).
pubmed: 29577577
doi: 10.1111/gbi.12285
Guy, R. D., Fogel, M. L. & Berry, J. A. Photosynthetic fractionation of the stable isotopes of oxygen and carbon. Plant Physiol. 101, 37–47 (1993).
pubmed: 12231663
pmcid: 158645
doi: 10.1104/pp.101.1.37
Garcia, A. K. et al. Effects of RuBisCO and CO
pubmed: 36602111
doi: 10.1111/gbi.12543
Hurley, S. J., Wing, B. A., Jasper, C. E., Hill, N. C. & Cameron, J. C. Carbon isotope evidence for the global physiology of Proterozoic cyanobacteria. Sci. Adv. 7, eabc8998 (2021).
pubmed: 33523966
pmcid: 7787495
doi: 10.1126/sciadv.abc8998
Laws, E. A., Popp, B. N., Bidigare, R. R., Kennicutt, M. C. & Macko, S. A. Dependence of phytoplankton carbon isotopic composition on growth rate and [CO
doi: 10.1016/0016-7037(95)00030-4
Des Marais, D. J., Strauss, H., Summons, R. E. & Hayes, J. M. Carbon isotope evidence for the stepwise oxidation of the Proterozoic environment. Nature 359, 605–609 (1992).
pubmed: 11536507
doi: 10.1038/359605a0
Hamilton, T. L., Bryant, D. A. & Macalady, J. L. The role of biology in planetary evolution: cyanobacterial primary production in low-oxygen Proterozoic oceans. Environ. Microbiol. 18, 325–340 (2016).
pubmed: 26549614
doi: 10.1111/1462-2920.13118
Freeman, K. H. & Hayes, J. M. Fractionation of carbon isotopes by phytoplankton and estimates of ancient CO
doi: 10.1029/92GB00190
Freeman, K. H., Hayes, J. M., Trendel, J.-M. & Albrecht, P. Evidence from carbon isotope measurements for diverse origins of sedimentary hydrocarbons. Nature 343, 254–256 (1990).
pubmed: 11536462
doi: 10.1038/343254a0
Hayes, J. M., Freeman, K. H., Popp, B. N. & Hoham, C. H. Compound-specific isotopic analyses: a novel tool for reconstruction of ancient biogeochemical processes. Org. Geochem. 16, 1115–1128 (1990).
pubmed: 11540919
doi: 10.1016/0146-6380(90)90147-R
Hayes, J. M. Fractionation of carbon and hydrogen isotopes in biosynthetic processes. Rev. Mineral. Geochem. 43, 225–277 (2001).
doi: 10.2138/gsrmg.43.1.225
van der Meer, M. T. J., Schouten, S. & Damsté, J. S. S. The effect of the reversed tricarboxylic acid cycle on the
doi: 10.1016/S0146-6380(98)00024-2
Crick, I. H., Boreham, C. J., Cook, A. C. & Powell, T. G. Petroleum geology and geochemistry of Middle Proterozoic McArthur Basin, Northern Australia II: assessment of source rock potential. AAPG Bull. 72, 1495–1514 (1988).
Meyer, K. M. & Kump, L. R. Oceanic Euxinia in Earth history: causes and consequences. Annu. Rev. Earth Planet. Sci. 36, 251–288 (2008).
doi: 10.1146/annurev.earth.36.031207.124256
Mukherjee, I. et al. Pyrite trace-element and sulfur isotope geochemistry of paleo-mesoproterozoic McArthur Basin: proxy for oxidative weathering. Am. Mineralogist: J. Earth Planet. Mater. 104, 1256–1272 (2019).
doi: 10.2138/am-2019-6873
Krissansen-Totton, J., Buick, R. & Catling, D. C. A statistical analysis of the carbon isotope record from the Archean to Phanerozoic and implications for the rise of oxygen. Am. J. Sci. 315, 275–316 (2015).
doi: 10.2475/04.2015.01
Brocks, J. J. & Schaeffer, P. Okenane, a biomarker for purple sulfur bacteria (Chromatiaceae), and other new carotenoid derivatives from the 1640 Ma Barney Creek Formation. Geochim. Cosmochim. Acta 72, 1396–1414 (2008).
doi: 10.1016/j.gca.2007.12.006
Sakata, S. et al. Carbon isotopic fractionation associated with lipid biosynthesis by a cyanobacterium: relevance for interpretation of biomarker records. Geochim. Cosmochim. Acta 61, 5379–5389 (1997).
pubmed: 11540730
doi: 10.1016/S0016-7037(97)00314-1
Brocks, J. J. The transition from a cyanobacterial to algal world and the emergence of animals. Emerg. Top. Life Sci. 2, 181–190 (2018).
pubmed: 32412625
doi: 10.1042/ETLS20180039
Graham, J. E. & Bryant, D. A. The biosynthetic pathway for synechoxanthin, an aromatic carotenoid synthesized by the euryhaline, unicellular cyanobacterium Synechococcus sp. strain PCC 7002. J. Bacteriol. 190, 7966–7974 (2008).
pubmed: 18849428
pmcid: 2593218
doi: 10.1128/JB.00985-08
French, K. L., Birdwell, J. E. & Berg, V. Biomarker similarities between the saline lacustrine Eocene Green River and the Paleoproterozoic Barney Creek Formations. Geochim. Cosmochim. Acta 274, 228–245 (2020).
doi: 10.1016/j.gca.2020.01.053
Smith, D. A., Steele, A., Bowden, R. & Fogel, M. L. Ecologically and geologically relevant isotope signatures of C, N, and S: okenone producing purple sulfur bacteria part I. Geobiology 13, 278–291 (2015).
pubmed: 25857753
doi: 10.1111/gbi.12136
Smith, D. A., Steele, A. & Fogel, M. L. Pigment production and isotopic fractionations in continuous culture: okenone producing purple sulfur bacteria Part II. Geobiology 13, 292–301 (2015).
pubmed: 25857754
doi: 10.1111/gbi.12135
Posth, N. R. et al. Carbon isotope fractionation by anoxygenic phototrophic bacteria in euxinic Lake Cadagno. Geobiology 15, 798–816 (2017).
pubmed: 28866873
doi: 10.1111/gbi.12254
Sattley, W. M. et al. Complete genome of the thermophilic purple sulfur bacterium Thermochromatium tepidum compared to Allochromatium vinosum and other Chromatiaceae. Photosynthesis Res. 151, 125–142 (2021).
Ohkouchi, N. et al. Biogeochemical processes in the saline meromictic Lake Kaiike, Japan: implications from molecular isotopic evidences of photosynthetic pigments. Environ. Microbiol. 7, 1009–1016 (2005).
pubmed: 15946297
doi: 10.1111/j.1462-2920.2005.00772.x
Hartgers, W. A., Schouten, S., Lopez, J. F., Damsté, J. S. S. & Grimalt, J. O.
doi: 10.1016/S0146-6380(00)00095-4
Schouten, S. et al. Molecular organic tracers of biogeochemical processes in a saline meromictic lake (Ace Lake). Geochim. Cosmochim. Acta 65, 1629–1640 (2001).
doi: 10.1016/S0016-7037(00)00627-X
Johnston, D. T., Wolfe-Simon, F., Pearson, A. & Knoll, A. H. Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age. Proc. Natl Acad. Sci. USA 106, 16925–16929 (2009).
pubmed: 19805080
pmcid: 2753640
doi: 10.1073/pnas.0909248106
Bryant, D. et al. in Functional Genomics and Evolution of Photosynthetic Systems Advances in Photosynthesis and Respiration Vol. 33 (eds Burnap, R. & Vermaas, W.) 47–102 (Springer, 2012).
Kah, L. C., Lyons, T. W. & Frank, T. D. Low marine sulphate and protracted oxygenation of the Proterozoic biosphere. Nature 431, 834–838 (2004).
pubmed: 15483609
doi: 10.1038/nature02974
Fakhraee, M., Hancisse, O., Canfield, D. E., Crowe, S. A. & Katsev, S. Proterozoic seawater sulfate scarcity and the evolution of ocean–atmosphere chemistry. Nat. Geosci. 12, 375–380 (2019).
doi: 10.1038/s41561-019-0351-5
Johnston, D. T. et al. Sulfur isotope biogeochemistry of the Proterozoic McArthur Basin. Geochim. Cosmochim. Acta 72, 4278–4290 (2008).
doi: 10.1016/j.gca.2008.06.004
Hamilton, T. L. et al. Coupled reductive and oxidative sulfur cycling in the phototrophic plate of a meromictic lake. Geobiology 12, 451–468 (2014).
pubmed: 24976102
doi: 10.1111/gbi.12092
Wilbanks, E. G. et al. Microscale sulfur cycling in the phototrophic pink berry consortia of the Sippewissett Salt Marsh. Environ. Microbiol. 16, 3398–3415 (2014).
pubmed: 24428801
pmcid: 4262008
doi: 10.1111/1462-2920.12388
Sinninghe Damsté, J. S., Van Duin, A. C. T., Hollander, D., Kohnen, M. E. L. & De Leeuw, J. W. Early diagenesis of bacteriohopanepolyol derivatives: formation of fossil homohopanoids. Geochim. Cosmochim. Acta 59, 5141–5157 (1995).
doi: 10.1016/0016-7037(95)00338-X
Birgel, D. et al. Lipid biomarker patterns of methane-seep microbialites from the Mesozoic convergent margin of California. Org. Geochem. 37, 1289–1302 (2006).
doi: 10.1016/j.orggeochem.2006.02.004
Brocks, J. J. et al. Lost world of complex life and the late rise of the eukaryotic crown. Nature 618, 767–773 (2023).
pubmed: 37286610
doi: 10.1038/s41586-023-06170-w
Tang, T. et al. Geochemically distinct carbon isotope distributions in Allochromatium vinosum DSM 180T grown photoautotrophically and photoheterotrophically. Geobiology 15, 324–339 (2017).
pubmed: 28042698
doi: 10.1111/gbi.12221
Logan, G. A., Hayes, J. M., Hieshima, G. B. & Summons, R. E. Terminal Proterozoic reorganization of biogeochemical cycles. Nature 376, 53–56 (1995).
pubmed: 11536694
doi: 10.1038/376053a0
Close, H. G., Bovee, R. & Pearson, A. Inverse carbon isotope patterns of lipids and kerogen record heterogeneous primary biomass. Geobiology 9, 250–265 (2011).
pubmed: 21366841
doi: 10.1111/j.1472-4669.2011.00273.x
Imhoff, J. F. in Sulfur Metabolism in Phototrophic Organisms Advances in Photosynthesis and Respiration Vol. 27 (eds Hell, R. et al.) 269–287 (Springer, 2008).
Liu, Z. et al. ‘Candidatus Thermochlorobacter aerophilum:’ an aerobic chlorophotoheterotrophic member of the phylum Chlorobi defined by metagenomics and metatranscriptomics. ISME J. 6, 1869–1882 (2012).
Stamps, B. W., Corsetti, F. A., Spear, J. R. & Stevenson, B. S. Draft genome of a novel Chlorobi member assembled by tetranucleotide binning of a hot spring metagenome. Genome Announce. Genome Announce. 2, e00897-14 (2014).
doi: 10.1128/genomeA.00897-14
Hoffman, P. F. The break-up of Rodinia, birth of Gondwana, true polar wander and the snowball Earth. J. Afr. Earth. Sci. 28, 17–33 (1999).
doi: 10.1016/S0899-5362(99)00018-4
Crockford, P. W. et al. Triple oxygen isotope evidence for limited mid-Proterozoic primary productivity. Nature 559, 613–616 (2018).
pubmed: 30022163
doi: 10.1038/s41586-018-0349-y
Hügler, M. & Sievert, S. M. Beyond the Calvin cycle: autotrophic carbon fixation in the ocean. Annu. Rev. Mar. Sci. 3, 261–289 (2011).
doi: 10.1146/annurev-marine-120709-142712
Page, R. W. & Sweet, I. P. Geochronology of basin phases in the western Mt Isa Inlier, and correlation with the McArthur Basin. Aust. J. Earth Sci. 45, 219–232 (1998).
doi: 10.1080/08120099808728383
Bull, S. W. Sedimentology of the Palaeoproterozoic Barney Creek formation in DDH BMR McArthur 2, southern McArthur basin, northern territory. Aust. J. Earth Sci. 45, 21–31 (1998).
doi: 10.1080/08120099808728364
Rawlings, D. J. Stratigraphic resolution of a multiphase intracratonic basin system: the McArthur Basin, northern Australia. Aust. J. Earth Sci. 46, 703–723 (1999).
doi: 10.1046/j.1440-0952.1999.00739.x
Jackson, M. J., Muir, M. D. & Plumb, K. A. Geology of the Southern McArthur Basin, Northern Territory Vol. 223 (Australian Government Pub. Service, 1987).
Jarrett, A. J. M., Schinteie, R., Hope, J. M. & Brocks, J. J. Micro-ablation, a new technique to remove drilling fluids and other contaminants from fragmented and fissile rock material. Org. Geochem. 61, 57–65 (2013).
doi: 10.1016/j.orggeochem.2013.06.005
Jiang, A., Zhou, P., Sun, Y. & Xie, L. Rapid column chromatography separation of alkylnaphthalenes from aromatic components in sedimentary organic matter for compound specific stable isotope analysis. Org. Geochem. 60, 1–8 (2013).
doi: 10.1016/j.orggeochem.2013.04.007
Ellis, L., Kagi, R. I. & Alexander, R. Separation of petroleum hydrocarbons using dealuminated mordenite molecular sieve. I. Monoaromatic hydrocarbons. Org. Geochem. 18, 587–593 (1992).
doi: 10.1016/0146-6380(92)90084-B
Kelly, A. E., Love, G. D., Zumberge, J. E. & Summons, R. E. Hydrocarbon biomarkers of Neoproterozoic to Lower Cambrian oils from eastern Siberia. Org. Geochem. 42, 640–654 (2011).
doi: 10.1016/j.orggeochem.2011.03.028
Summons, R. E. & Powell, T. G. Identification of aryl isoprenoids in source rocks and crude oils: biological markers for the green sulphur bacteria. Geochim. Cosmochim. Acta 51, 557–566 (1987).
doi: 10.1016/0016-7037(87)90069-X
Harris, D., Horwáth, W. R. & Van Kessel, C. Acid fumigation of soils to remove carbonates prior to total organic carbon or carbon‐13 isotopic analysis. Soil Sci. Soc. Am. J. 65, 1853–1856 (2001).
doi: 10.2136/sssaj2001.1853