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. 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.
    3. 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.
    4. 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.
    5. 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.
    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. Daniel R. Colman & Lisa M. Keller & Emilia Arteaga-Pozo & Eva Andrade-Barahona & Brian Clair & Anna Shoemaker & Alysia Cox & Eric S. Boyd, 2024. "Covariation of hot spring geochemistry with microbial genomic diversity, function, and evolution," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    2. 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.
    3. 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.
    4. Minghui Cheng & Yingjie Xu & Xiao Cui & Xin Wei & Yundi Chang & Jun Xu & Cheng Lei & Lei Xue & Yifan Zheng & Zhang Wang & Lingtong Huang & Min Zheng & Hong Luo & Yuxin Leng & Chao Jiang, 2024. "Deep longitudinal lower respiratory tract microbiome profiling reveals genome-resolved functional and evolutionary dynamics in critical illness," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. 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.
    6. Jiandui Mi & Xiaoping Jing & Chouxian Ma & Fuyu Shi & Ze Cao & Xin Yang & Yiwen Yang & Apurva Kakade & Weiwei Wang & Ruijun Long, 2024. "A metagenomic catalogue of the ruminant gut archaeome," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Yan-Ling Qi & Ya-Ting Chen & Yuan-Guo Xie & Yu-Xian Li & Yang-Zhi Rao & Meng-Meng Li & Qi-Jun Xie & Xing-Ru Cao & Lei Chen & Yan-Ni Qu & Zhen-Xuan Yuan & Zhi-Chao Xiao & Lu Lu & Jian-Yu Jiao & Wen-She, 2024. "Analysis of nearly 3000 archaeal genomes from terrestrial geothermal springs sheds light on interconnected biogeochemical processes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Vincent Somerville & Nadine Thierer & Remo S. Schmidt & Alexandra Roetschi & Lauriane Braillard & Monika Haueter & Hélène Berthoud & Noam Shani & Ueli Ah & Florent Mazel & Philipp Engel, 2024. "Genomic and phenotypic imprints of microbial domestication on cheese starter cultures," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Jordy Evan Sulaiman & Jaron Thompson & Yili Qian & Eugenio I. Vivas & Christian Diener & Sean M. Gibbons & Nasia Safdar & Ophelia S. Venturelli, 2024. "Elucidating human gut microbiota interactions that robustly inhibit diverse Clostridioides difficile strains across different nutrient landscapes," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    10. 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.
    11. 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.
    12. Lucas Serra Moncadas & Cyrill Hofer & Paul-Adrian Bulzu & Jakob Pernthaler & Adrian-Stefan Andrei, 2024. "Freshwater genome-reduced bacteria exhibit pervasive episodes of adaptive stasis," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. 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.
    14. 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.
    15. 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.
    16. Wei Ding & Shougang Wang & Peng Qin & Shen Fan & Xiaoyan Su & Peiyan Cai & Jie Lu & Han Cui & Meng Wang & Yi Shu & Yongming Wang & Hui-Hui Fu & Yu-Zhong Zhang & Yong-Xin Li & Weipeng Zhang, 2023. "Anaerobic thiosulfate oxidation by the Roseobacter group is prevalent in marine biofilms," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    17. 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.
    18. Roxana Zamudio & Patrick Boerlin & Racha Beyrouthy & Jean-Yves Madec & Stefan Schwarz & Michael R. Mulvey & George G. Zhanel & Ashley Cormier & Gabhan Chalmers & Richard Bonnet & Marisa Haenni & Inga , 2022. "Dynamics of extended-spectrum cephalosporin resistance genes in Escherichia coli from Europe and North America," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. 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.
    20. 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.

    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.