Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions

Lian Narunsky-Haziza; Gregory D. Sepich-Poore; Ilana Livyatan; Omer Asraf; Cameron Martino; Deborah Nejman; Nancy Gavert; Jason E. Stajich; Guy Amit; Antonio González; Stephen Wandro; Gili Perry; Ruthie Ariel; Arnon Meltser; Justin P. Shaffer; Qiyun Zhu; Nora Balint-Lahat; Iris Barshack; Maya Dadiani; Einav N. Gal-Yam; Sandip Pravin Patel; Amir Bashan; Austin D. Swafford; Yitzhak Pilpel; Rob Knight; Ravid Straussman

doi:10.1016/j.cell.2022.09.005

Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions

Lian Narunsky-Haziza, Gregory D. Sepich-Poore, Ilana Livyatan, Omer Asraf, Cameron Martino, Deborah Nejman, Nancy Gavert, Jason E. Stajich, Guy Amit, Antonio González, Stephen Wandro, Gili Perry, Ruthie Ariel, Arnon Meltser, Justin P. Shaffer, Qiyun Zhu, Nora Balint-Lahat, Iris Barshack, Maya Dadiani, Einav N. Gal-YamSandip Pravin Patel, Amir Bashan, Austin D. Swafford, Yitzhak Pilpel, Rob Knight, Ravid Straussman

Life Sciences, School of (SOLS)

Research output: Contribution to journal › Article › peer-review

140 Scopus citations

Abstract

Cancer-microbe associations have been explored for centuries, but cancer-associated fungi have rarely been examined. Here, we comprehensively characterize the cancer mycobiome within 17,401 patient tissue, blood, and plasma samples across 35 cancer types in four independent cohorts. We report fungal DNA and cells at low abundances across many major human cancers, with differences in community compositions that differ among cancer types, even when accounting for technical background. Fungal histological staining of tissue microarrays supported intratumoral presence and frequent spatial association with cancer cells and macrophages. Comparing intratumoral fungal communities with matched bacteriomes and immunomes revealed co-occurring bi-domain ecologies, often with permissive, rather than competitive, microenvironments and distinct immune responses. Clinically focused assessments suggested prognostic and diagnostic capacities of the tissue and plasma mycobiomes, even in stage I cancers, and synergistic predictive performance with bacteriomes.

Original language	English (US)
Pages (from-to)	3789-3806.e17
Journal	Cell
Volume	185
Issue number	20
DOIs	https://doi.org/10.1016/j.cell.2022.09.005
State	Published - Sep 29 2022

Keywords

biomarkers
cancer
fungi
liquid biopsy
metagenomics
metatranscriptomics
microbial interactions
tumor microbiome
tumor mycobiome

ASJC Scopus subject areas

General Biochemistry, Genetics and Molecular Biology

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10.1016/j.cell.2022.09.005

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Narunsky-Haziza, L., Sepich-Poore, G. D., Livyatan, I., Asraf, O., Martino, C., Nejman, D., Gavert, N., Stajich, J. E., Amit, G., González, A., Wandro, S., Perry, G., Ariel, R., Meltser, A., Shaffer, J. P., Zhu, Q., Balint-Lahat, N., Barshack, I., Dadiani, M., ... Straussman, R. (2022). Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions. Cell, 185(20), 3789-3806.e17. https://doi.org/10.1016/j.cell.2022.09.005

Narunsky-Haziza, L, Sepich-Poore, GD, Livyatan, I, Asraf, O, Martino, C, Nejman, D, Gavert, N, Stajich, JE, Amit, G, González, A, Wandro, S, Perry, G, Ariel, R, Meltser, A, Shaffer, JP, Zhu, Q, Balint-Lahat, N, Barshack, I, Dadiani, M, Gal-Yam, EN, Patel, SP, Bashan, A, Swafford, AD, Pilpel, Y, Knight, R & Straussman, R 2022, 'Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions', Cell, vol. 185, no. 20, pp. 3789-3806.e17. https://doi.org/10.1016/j.cell.2022.09.005

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abstract = "Cancer-microbe associations have been explored for centuries, but cancer-associated fungi have rarely been examined. Here, we comprehensively characterize the cancer mycobiome within 17,401 patient tissue, blood, and plasma samples across 35 cancer types in four independent cohorts. We report fungal DNA and cells at low abundances across many major human cancers, with differences in community compositions that differ among cancer types, even when accounting for technical background. Fungal histological staining of tissue microarrays supported intratumoral presence and frequent spatial association with cancer cells and macrophages. Comparing intratumoral fungal communities with matched bacteriomes and immunomes revealed co-occurring bi-domain ecologies, often with permissive, rather than competitive, microenvironments and distinct immune responses. Clinically focused assessments suggested prognostic and diagnostic capacities of the tissue and plasma mycobiomes, even in stage I cancers, and synergistic predictive performance with bacteriomes.",

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AU - Narunsky-Haziza, Lian

AU - Sepich-Poore, Gregory D.

AU - Livyatan, Ilana

AU - Asraf, Omer

AU - Martino, Cameron

AU - Nejman, Deborah

AU - Gavert, Nancy

AU - Stajich, Jason E.

AU - Amit, Guy

AU - González, Antonio

AU - Wandro, Stephen

AU - Perry, Gili

AU - Ariel, Ruthie

AU - Meltser, Arnon

AU - Shaffer, Justin P.

AU - Zhu, Qiyun

AU - Balint-Lahat, Nora

AU - Barshack, Iris

AU - Dadiani, Maya

AU - Gal-Yam, Einav N.

AU - Patel, Sandip Pravin

AU - Bashan, Amir

AU - Swafford, Austin D.

AU - Pilpel, Yitzhak

AU - Knight, Rob

AU - Straussman, Ravid

PY - 2022/9/29

Y1 - 2022/9/29

N2 - Cancer-microbe associations have been explored for centuries, but cancer-associated fungi have rarely been examined. Here, we comprehensively characterize the cancer mycobiome within 17,401 patient tissue, blood, and plasma samples across 35 cancer types in four independent cohorts. We report fungal DNA and cells at low abundances across many major human cancers, with differences in community compositions that differ among cancer types, even when accounting for technical background. Fungal histological staining of tissue microarrays supported intratumoral presence and frequent spatial association with cancer cells and macrophages. Comparing intratumoral fungal communities with matched bacteriomes and immunomes revealed co-occurring bi-domain ecologies, often with permissive, rather than competitive, microenvironments and distinct immune responses. Clinically focused assessments suggested prognostic and diagnostic capacities of the tissue and plasma mycobiomes, even in stage I cancers, and synergistic predictive performance with bacteriomes.

AB - Cancer-microbe associations have been explored for centuries, but cancer-associated fungi have rarely been examined. Here, we comprehensively characterize the cancer mycobiome within 17,401 patient tissue, blood, and plasma samples across 35 cancer types in four independent cohorts. We report fungal DNA and cells at low abundances across many major human cancers, with differences in community compositions that differ among cancer types, even when accounting for technical background. Fungal histological staining of tissue microarrays supported intratumoral presence and frequent spatial association with cancer cells and macrophages. Comparing intratumoral fungal communities with matched bacteriomes and immunomes revealed co-occurring bi-domain ecologies, often with permissive, rather than competitive, microenvironments and distinct immune responses. Clinically focused assessments suggested prognostic and diagnostic capacities of the tissue and plasma mycobiomes, even in stage I cancers, and synergistic predictive performance with bacteriomes.

KW - biomarkers

KW - cancer

KW - fungi

KW - liquid biopsy

KW - metagenomics

KW - metatranscriptomics

KW - microbial interactions

KW - tumor microbiome

KW - tumor mycobiome

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Pan-cancer analyses reveal cancer-type-specific fungal ecologies and bacteriome interactions

Abstract

Keywords

ASJC Scopus subject areas

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