Literature DB >> 34285074

Termite gas emissions select for hydrogenotrophic microbial communities in termite mounds.

Eleonora Chiri1,2, Philipp A Nauer3,4, Rachael Lappan2, Thanavit Jirapanjawat1, David W Waite5,6, Kim M Handley5, Philip Hugenholtz6, Perran L M Cook4, Stefan K Arndt2, Chris Greening7.   

Abstract

Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H2), levels of this gas are generally insufficient to sustain hydrogenotrophic growth. In contrast, bacteria residing within soil-derived termite mounds are exposed to high fluxes of H2 due to fermentative production within termite guts. Here, we show through community, metagenomic, and biogeochemical profiling that termite emissions select for a community dominated by diverse hydrogenotrophic Actinobacteriota and Dormibacterota. Based on metagenomic short reads and derived genomes, uptake hydrogenase and chemosynthetic RuBisCO genes were significantly enriched in mounds compared to surrounding soils. In situ and ex situ measurements confirmed that high- and low-affinity H2-oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H2 emissions and served as net sinks of atmospheric H2 Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H2 oxidation rates (R 2 = 0.82). Cell-specific power calculations confirmed the potential for hydrogenotrophic growth in the mounds with most termite activity. In contrast, while methane is produced at similar rates to H2 by termites, mounds contained few methanotrophs and were net sources of methane. Altogether, these findings provide further evidence of a highly responsive terrestrial sink for H2 but not methane and suggest H2 availability shapes composition and activity of microbial communities. They also reveal a unique arthropod-bacteria interaction dependent on H2 transfer between host-associated and free-living microbial communities.

Entities:  

Keywords:  Actinobacteria; hydrogen; lithoautotrophy; termite; trace gas

Mesh:

Substances:

Year:  2021        PMID: 34285074      PMCID: PMC8325338          DOI: 10.1073/pnas.2102625118

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  48 in total

1.  Termites: a potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen.

Authors:  P R Zimmerman; J P Greenberg; S O Wandiga; P J Crutzen
Journal:  Science       Date:  1982-11-05       Impact factor: 47.728

2.  Consumption of atmospheric hydrogen during the life cycle of soil-dwelling actinobacteria.

Authors:  Laura K Meredith; Deepa Rao; Tanja Bosak; Vanja Klepac-Ceraj; Kendall R Tada; Colleen M Hansel; Shuhei Ono; Ronald G Prinn
Journal:  Environ Microbiol Rep       Date:  2013-11-20       Impact factor: 3.541

3.  Fast and sensitive protein alignment using DIAMOND.

Authors:  Benjamin Buchfink; Chao Xie; Daniel H Huson
Journal:  Nat Methods       Date:  2014-11-17       Impact factor: 28.547

Review 4.  Embracing the unknown: disentangling the complexities of the soil microbiome.

Authors:  Noah Fierer
Journal:  Nat Rev Microbiol       Date:  2017-08-21       Impact factor: 60.633

5.  High-resolution analysis of gut environment and bacterial microbiota reveals functional compartmentation of the gut in wood-feeding higher termites (Nasutitermes spp.).

Authors:  Tim Köhler; Carsten Dietrich; Rudolf H Scheffrahn; Andreas Brune
Journal:  Appl Environ Microbiol       Date:  2012-04-27       Impact factor: 4.792

6.  Atmospheric trace gases support primary production in Antarctic desert surface soil.

Authors:  Mukan Ji; Chris Greening; Inka Vanwonterghem; Carlo R Carere; Sean K Bay; Jason A Steen; Kate Montgomery; Thomas Lines; John Beardall; Josie van Dorst; Ian Snape; Matthew B Stott; Philip Hugenholtz; Belinda C Ferrari
Journal:  Nature       Date:  2017-12-06       Impact factor: 49.962

7.  H2 metabolism is widespread and diverse among human colonic microbes.

Authors:  Patricia G Wolf; Ambarish Biswas; Sergio E Morales; Chris Greening; H Rex Gaskins
Journal:  Gut Microbes       Date:  2016-05-03

8.  Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide.

Authors:  Zahra F Islam; Paul R F Cordero; Joanna Feng; Ya-Jou Chen; Sean K Bay; Thanavit Jirapanjawat; Roslyn M Gleadow; Carlo R Carere; Matthew B Stott; Eleonora Chiri; Chris Greening
Journal:  ISME J       Date:  2019-03-14       Impact factor: 10.302

9.  Termite mounds contain soil-derived methanotroph communities kinetically adapted to elevated methane concentrations.

Authors:  Eleonora Chiri; Philipp A Nauer; Chris Greening; Rachael Lappan; David W Waite; Thanavit Jirapanjawat; Xiyang Dong; Stefan K Arndt
Journal:  ISME J       Date:  2020-07-24       Impact factor: 10.302

10.  Acidobacteria are active and abundant members of diverse atmospheric H2-oxidizing communities detected in temperate soils.

Authors:  Andrew T Giguere; Stephanie A Eichorst; Dimitri V Meier; Craig W Herbold; Andreas Richter; Chris Greening; Dagmar Woebken
Journal:  ISME J       Date:  2020-10-06       Impact factor: 10.302

View more
  1 in total

Review 1.  Microbial oxidation of atmospheric trace gases.

Authors:  Chris Greening; Rhys Grinter
Journal:  Nat Rev Microbiol       Date:  2022-04-12       Impact factor: 78.297

  1 in total

北京卡尤迪生物科技股份有限公司 © 2022-2023.