IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-43960-2.html
   My bibliography  Save this article

A genus in the bacterial phylum Aquificota appears to be endemic to Aotearoa-New Zealand

Author

Listed:
  • Jean F. Power

    (Te Whare Wānanga o Waikato | University of Waikato)

  • Carlo R. Carere

    (Te Whare Wānanga o Waitaha | University of Canterbury)

  • Holly E. Welford

    (Te Whare Wānanga o Waitaha | University of Canterbury)

  • Daniel T. Hudson

    (Te Whare Wānanga o Ōtākou | University of Otago)

  • Kevin C. Lee

    (Te Wānanga Aronui o Tāmaki Makau Rau | Auckland University of Technology)

  • John W. Moreau

    (University of Glasgow)

  • Thijs J. G. Ettema

    (Wageningen University & Research)

  • Anna-Louise Reysenbach

    (Portland State University)

  • Charles K. Lee

    (Te Whare Wānanga o Waikato | University of Waikato)

  • Daniel R. Colman

    (Montana State University)

  • Eric S. Boyd

    (Montana State University)

  • Xochitl C. Morgan

    (Te Whare Wānanga o Ōtākou | University of Otago
    Harvard T. H. Chan School of Public Health)

  • Ian R. McDonald

    (Te Whare Wānanga o Waikato | University of Waikato)

  • S. Craig Cary

    (Te Whare Wānanga o Waikato | University of Waikato)

  • Matthew B. Stott

    (Te Whare Wānanga o Waitaha | University of Canterbury)

Abstract

Allopatric speciation has been difficult to examine among microorganisms, with prior reports of endemism restricted to sub-genus level taxa. Previous microbial community analysis via 16S rRNA gene sequencing of 925 geothermal springs from the Taupō Volcanic Zone (TVZ), Aotearoa-New Zealand, revealed widespread distribution and abundance of a single bacterial genus across 686 of these ecosystems (pH 1.2-9.6 and 17.4-99.8 °C). Here, we present evidence to suggest that this genus, Venenivibrio (phylum Aquificota), is endemic to Aotearoa-New Zealand. A specific environmental niche that increases habitat isolation was identified, with maximal read abundance of Venenivibrio occurring at pH 4-6, 50-70 °C, and low oxidation-reduction potentials. This was further highlighted by genomic and culture-based analyses of the only characterised species for the genus, Venenivibrio stagnispumantis CP.B2T, which confirmed a chemolithoautotrophic metabolism dependent on hydrogen oxidation. While similarity between Venenivibrio populations illustrated that dispersal is not limited across the TVZ, extensive amplicon, metagenomic, and phylogenomic analyses of global microbial communities from DNA sequence databases indicates Venenivibrio is geographically restricted to the Aotearoa-New Zealand archipelago. We conclude that geographic isolation, complemented by physicochemical constraints, has resulted in the establishment of an endemic bacterial genus.

Suggested Citation

  • Jean F. Power & Carlo R. Carere & Holly E. Welford & Daniel T. Hudson & Kevin C. Lee & John W. Moreau & Thijs J. G. Ettema & Anna-Louise Reysenbach & Charles K. Lee & Daniel R. Colman & Eric S. Boyd &, 2024. "A genus in the bacterial phylum Aquificota appears to be endemic to Aotearoa-New Zealand," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43960-2
    DOI: 10.1038/s41467-023-43960-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43960-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43960-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Chirag Jain & Luis M. Rodriguez-R & Adam M. Phillippy & Konstantinos T. Konstantinidis & Srinivas Aluru, 2018. "High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    2. Hong Qian & Robert E. Ricklefs, 2000. "Large-scale processes and the Asian bias in species diversity of temperate plants," Nature, Nature, vol. 407(6801), pages 180-182, September.
    3. Jean F. Power & Carlo R. Carere & Charles K. Lee & Georgia L. J. Wakerley & David W. Evans & Mathew Button & Duncan White & Melissa D. Climo & Annika M. Hinze & Xochitl C. Morgan & Ian R. McDonald & S, 2018. "Microbial biogeography of 925 geothermal springs in New Zealand," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    4. Daniel R. Colman & Melody R. Lindsay & Eric S. Boyd, 2019. "Mixing of meteoric and geothermal fluids supports hyperdiverse chemosynthetic hydrothermal communities," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    5. Craig W. Herbold & Charles K. Lee & Ian R. McDonald & S. Craig Cary, 2014. "Evidence of global-scale aeolian dispersal and endemism in isolated geothermal microbial communities of Antarctica," Nature Communications, Nature, vol. 5(1), pages 1-10, September.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. M. C. Rühlemann & C. Bang & J. F. Gogarten & B. M. Hermes & M. Groussin & S. Waschina & M. Poyet & M. Ulrich & C. Akoua-Koffi & T. Deschner & J. J. Muyembe-Tamfum & M. M. Robbins & M. Surbeck & R. M. , 2024. "Functional host-specific adaptation of the intestinal microbiome in hominids," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Ling Zhong & Menghan Zhang & Libing Sun & Yu Yang & Bo Wang & Haibing Yang & Qiang Shen & Yu Xia & Jiarui Cui & Hui Hang & Yi Ren & Bo Pang & Xiangyu Deng & Yahui Zhan & Heng Li & Zhemin Zhou, 2023. "Distributed genotyping and clustering of Neisseria strains reveal continual emergence of epidemic meningococcus over a century," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Aleksandar Stanojković & Svatopluk Skoupý & Hanna Johannesson & Petr Dvořák, 2024. "The global speciation continuum of the cyanobacterium Microcoleus," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    4. Pok Man Leung & Rhys Grinter & Eve Tudor-Matthew & James P. Lingford & Luis Jimenez & Han-Chung Lee & Michael Milton & Iresha Hanchapola & Erwin Tanuwidjaya & Ashleigh Kropp & Hanna A. Peach & Carlo R, 2024. "Trace gas oxidation sustains energy needs of a thermophilic archaeon at suboptimal temperatures," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Xin Fan & Rong-Chen Dai & Shu Zhang & Yuan-Yuan Geng & Mei Kang & Da-Wen Guo & Ya-Ning Mei & Yu-Hong Pan & Zi-Yong Sun & Ying-Chun Xu & Jie Gong & Meng Xiao, 2023. "Tandem gene duplications contributed to high-level azole resistance in a rapidly expanding Candida tropicalis population," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    6. Lucie Semenec & Amy K. Cain & Catherine J. Dawson & Qi Liu & Hue Dinh & Hannah Lott & Anahit Penesyan & Ram Maharjan & Francesca L. Short & Karl A. Hassan & Ian T. Paulsen, 2023. "Cross-protection and cross-feeding between Klebsiella pneumoniae and Acinetobacter baumannii promotes their co-existence," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Corentin Hochart & Lucas Paoli & Hans-Joachim Ruscheweyh & Guillem Salazar & Emilie Boissin & Sarah Romac & Julie Poulain & Guillaume Bourdin & Guillaume Iwankow & Clémentine Moulin & Maren Ziegler & , 2023. "Ecology of Endozoicomonadaceae in three coral genera across the Pacific Ocean," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Daniel P. Morreale & Eric A. Porsch & Brad K. Kern & Joseph W. Geme & Paul J. Planet, 2023. "Acquisition, co-option, and duplication of the rtx toxin system and the emergence of virulence in Kingella," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    9. Xiyang Dong & Yongyi Peng & Muhua Wang & Laura Woods & Wenxue Wu & Yong Wang & Xi Xiao & Jiwei Li & Kuntong Jia & Chris Greening & Zongze Shao & Casey R. J. Hubert, 2023. "Evolutionary ecology of microbial populations inhabiting deep sea sediments associated with cold seeps," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    10. Xuanji Li & Asker Brejnrod & Jonathan Thorsen & Trine Zachariasen & Urvish Trivedi & Jakob Russel & Gisle Alberg Vestergaard & Jakob Stokholm & Morten Arendt Rasmussen & Søren Johannes Sørensen, 2023. "Differential responses of the gut microbiome and resistome to antibiotic exposures in infants and adults," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    11. Hannah B. Rappaport & Angela M. Oliverio, 2023. "Extreme environments offer an unprecedented opportunity to understand microbial eukaryotic ecology, evolution, and genome biology," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Sanjam S. Sawhney & Rhiannon C. Vargas & Meghan A. Wallace & Carol E. Muenks & Brian V. Lubbers & Stephanie A. Fritz & Carey-Ann D. Burnham & Gautam Dantas, 2023. "Diagnostic and commensal Staphylococcus pseudintermedius genomes reveal niche adaptation through parallel selection of defense mechanisms," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    13. Harold P. Hodgins & Pengsheng Chen & Briallen Lobb & Xin Wei & Benjamin J. M. Tremblay & Michael J. Mansfield & Victoria C. Y. Lee & Pyung-Gang Lee & Jeffrey Coffin & Ana T. Duggan & Alexis E. Dolphin, 2023. "Ancient Clostridium DNA and variants of tetanus neurotoxins associated with human archaeological remains," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    14. Conor Feehily & Ian J. O’Neill & Calum J. Walsh & Rebecca L. Moore & Sarah Louise Killeen & Aisling A. Geraghty & Elaine M. Lawton & David Byrne & Rocio Sanchez-Gallardo & Sai Ravi Chandra Nori & Ida , 2023. "Detailed mapping of Bifidobacterium strain transmission from mother to infant via a dual culture-based and metagenomic approach," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Yuval Bussi & Ruti Kapon & Ziv Reich, 2021. "Large-scale k-mer-based analysis of the informational properties of genomes, comparative genomics and taxonomy," PLOS ONE, Public Library of Science, vol. 16(10), pages 1-27, October.
    16. Max E. Schön & Vasily V. Zlatogursky & Rohan P. Singh & Camille Poirier & Susanne Wilken & Varsha Mathur & Jürgen F. H. Strassert & Jarone Pinhassi & Alexandra Z. Worden & Patrick J. Keeling & Thijs J, 2021. "Single cell genomics reveals plastid-lacking Picozoa are close relatives of red algae," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    17. Nenad Macesic & Jane Hawkey & Ben Vezina & Jessica A. Wisniewski & Hugh Cottingham & Luke V. Blakeway & Taylor Harshegyi & Katherine Pragastis & Gnei Zweena Badoordeen & Amanda Dennison & Denis W. Spe, 2023. "Genomic dissection of endemic carbapenem resistance reveals metallo-beta-lactamase dissemination through clonal, plasmid and integron transfer," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    18. Jean-Sebastien Gounot & Minghao Chia & Denis Bertrand & Woei-Yuh Saw & Aarthi Ravikrishnan & Adrian Low & Yichen Ding & Amanda Hui Qi Ng & Linda Wei Lin Tan & Yik-Ying Teo & Henning Seedorf & Niranjan, 2022. "Genome-centric analysis of short and long read metagenomes reveals uncharacterized microbiome diversity in Southeast Asians," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    19. Ruobing Wang & Anru Zhang & Shijun Sun & Guankun Yin & Xingyu Wu & Qi Ding & Qi Wang & Fengning Chen & Shuyi Wang & Lucy Dorp & Yawei Zhang & Longyang Jin & Xiaojuan Wang & Francois Balloux & Hui Wang, 2024. "Increase in antioxidant capacity associated with the successful subclone of hypervirulent carbapenem-resistant Klebsiella pneumoniae ST11-KL64," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    20. Nils Giordano & Marinna Gaudin & Camille Trottier & Erwan Delage & Charlotte Nef & Chris Bowler & Samuel Chaffron, 2024. "Genome-scale community modelling reveals conserved metabolic cross-feedings in epipelagic bacterioplankton communities," Nature Communications, Nature, vol. 15(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-43960-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.