HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi

Nuccio, Erin E.; Blazewicz, Steven J.; Lafler, Marissa; Campbell, Ashley N.; Kakouridis, Anne; Kimbrel, Jeffrey A.; Wollard, Jessica; Vyshenska, Dariia; Riley, Robert; Tomatsu, Andy; Hestrin, Rachel; Malmstrom, Rex R.; Firestone, Mary; Pett-Ridge, Jennifer

doi:10.1186/s40168-022-01391-z

Title: HT-SIP: a semi-automated stable isotope probing pipeline identifies cross-kingdom interactions in the hyphosphere of arbuscular mycorrhizal fungi

Journal Article · Fri Nov 25 00:00:00 EST 2022 · Microbiome

DOI:https://doi.org/10.1186/s40168-022-01391-z· OSTI ID:1899808

Nuccio, Erin E.; Blazewicz, Steven J.; Lafler, Marissa; Campbell, Ashley N.; Kakouridis, Anne; Kimbrel, Jeffrey A.; Wollard, Jessica; Vyshenska, Dariia; Riley, Robert; Tomatsu, Andy; Hestrin, Rachel; Malmstrom, Rex R.; Firestone, Mary; Pett-Ridge, Jennifer

Background: Linking the identity of wild microbes with their ecophysiological traits and environmental functions is a key ambition for microbial ecologists. Of many techniques that strive for this goal, Stable-isotope probing—SIP—remains among the most comprehensive for studying whole microbial communities in situ. In DNA-SIP, actively growing microorganisms that take up an isotopically heavy substrate build heavier DNA, which can be partitioned by density into multiple fractions and sequenced. However, SIP is relatively low throughput and requires significant hands-on labor. We designed and tested a semi-automated, high-throughput SIP (HT-SIP) pipeline to support well-replicated, temporally resolved amplicon and metagenomics experiments. We applied this pipeline to a soil microhabitat with significant ecological importance—the hyphosphere zone surrounding arbuscular mycorrhizal fungal (AMF) hyphae. AMF form symbiotic relationships with most plant species and play key roles in terrestrial nutrient and carbon cycling. Results: Our HT-SIP pipeline for fractionation, cleanup, and nucleic acid quantification of density gradients requires one-sixth of the hands-on labor compared to manual SIP and allows 16 samples to be processed simultaneously. Automated density fractionation increased the reproducibility of SIP gradients compared to manual fractionation, and we show adding a non-ionic detergent to the gradient buffer improved SIP DNA recovery. We applied HT-SIP to ¹³C-AMF hyphosphere DNA from a ¹³CO₂ plant labeling study and created metagenome-assembled genomes (MAGs) using high-resolution SIP metagenomics (14 metagenomes per gradient). SIP confirmed the AMF Rhizophagus intraradices and associated MAGs were highly enriched (10–33 atom% 13C), even though the soils’ overall enrichment was low (1.8 atom% ¹³C). We assembled 212 ¹³C-hyphosphere MAGs; the hyphosphere taxa that assimilated the most AMF-derived ¹³C were from the phyla Myxococcota, Fibrobacterota, Verrucomicrobiota, and the ammonia-oxidizing archaeon genus Nitrososphaera. Conclusions: Our semi-automated HT-SIP approach decreases operator time and improves reproducibility by targeting the most labor-intensive steps of SIP—fraction collection and cleanup. We illustrate this approach in a unique and understudied soil microhabitat—generating MAGs of actively growing microbes living in the AMF hyphosphere (without plant roots). The MAGs’ phylogenetic composition and gene content suggest predation, decomposition, and ammonia oxidation may be key processes in hyphosphere nutrient cycling.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: SCW1711; SC0016247; SWC1632; AC02-05CH11231; AC52-07NA27344; SC0020163

OSTI ID:: 1899808

Alternate ID(s):: OSTI ID: 1903568; OSTI ID: 2203317

Report Number(s):: LLNL-JRNL-837051; 199; PII: 1391

Journal Information:: Microbiome, Journal Name: Microbiome Vol. 10 Journal Issue: 1; ISSN 2049-2618

Publisher:: Springer Science + Business MediaCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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