Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors

The paucity of microbiome studies at intestinal tissues has contributed to a yet limited understanding of potential viral and bacterial cofactors of colorectal cancer (CRC) carcinogenesis or progression. We analysed whole‐genome sequences of CRC primary tumours, their corresponding metastases and ma...

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Autores principales:	Luigi Marongiu, Jonathan J. M. Landry, Tobias Rausch, Mohammed L. Abba, Susanne Delecluse, Henri‐Jacques Delecluse, Heike Allgayer
Formato:	article
Lenguaje:	EN
Publicado:	Wiley 2021
Materias:	bacteriome colorectal cancer metastasis phages viruses Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282
Acceso en línea:	https://doaj.org/article/7de803998014476aa150c199a99be616
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spelling	oai:doaj.org-article:7de803998014476aa150c199a99be6162021-12-02T10:31:06ZMetagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors1878-02611574-789110.1002/1878-0261.13070https://doaj.org/article/7de803998014476aa150c199a99be6162021-12-01T00:00:00Zhttps://doi.org/10.1002/1878-0261.13070https://doaj.org/toc/1574-7891https://doaj.org/toc/1878-0261The paucity of microbiome studies at intestinal tissues has contributed to a yet limited understanding of potential viral and bacterial cofactors of colorectal cancer (CRC) carcinogenesis or progression. We analysed whole‐genome sequences of CRC primary tumours, their corresponding metastases and matched normal tissue for sequences of viral, phage and bacterial species. Bacteriome analysis showed Fusobacterium nucleatum, Streptococcus sanguinis, F. Hwasookii, Anaerococcus mediterraneensis and further species enriched in primary CRCs. The primary CRC of one patient was enriched for F. alocis, S. anginosus, Parvimonas micra and Gemella sp. 948. Enrichment of Escherichia coli strains IAI1, SE11, K‐12 and M8 was observed in metastases together with coliphages enterobacteria phage φ80 and Escherichia phage VT2φ_272. Virome analysis showed that phages were the most preponderant viral species (46%), the main families being Myoviridae, Siphoviridae and Podoviridae. Primary CRCs were enriched for bacteriophages, showing five phages (Enterobacteria, Bacillus, Proteus, Streptococcus phages) together with their pathogenic hosts in contrast to normal tissues. The most frequently detected, and Blast‐confirmed, viruses included human endogenous retrovirus K113, human herpesviruses 7 and 6B, Megavirus chilensis, cytomegalovirus (CMV) and Epstein–Barr virus (EBV), with one patient showing EBV enrichment in primary tumour and metastases. EBV was PCR‐validated in 80 pairs of CRC primary tumour and their corresponding normal tissues; in 21 of these pairs (26.3%), it was detectable in primary tumours only. The number of viral species was increased and bacterial species decreased in CRCs compared with normal tissues, and we could discriminate primary CRCs from metastases and normal tissues by applying the Hutcheson t‐test on the Shannon indices based on viral and bacterial species. Taken together, our results descriptively support hypotheses on microorganisms as potential (co)risk factors of CRC and extend putative suggestions on critical microbiome species in CRC metastasis.Luigi MarongiuJonathan J. M. LandryTobias RauschMohammed L. AbbaSusanne DelecluseHenri‐Jacques DelecluseHeike AllgayerWileyarticlebacteriomecolorectal cancermetastasisphagesvirusesNeoplasms. Tumors. Oncology. Including cancer and carcinogensRC254-282ENMolecular Oncology, Vol 15, Iss 12, Pp 3363-3384 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	bacteriome colorectal cancer metastasis phages viruses Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282
spellingShingle	bacteriome colorectal cancer metastasis phages viruses Neoplasms. Tumors. Oncology. Including cancer and carcinogens RC254-282 Luigi Marongiu Jonathan J. M. Landry Tobias Rausch Mohammed L. Abba Susanne Delecluse Henri‐Jacques Delecluse Heike Allgayer Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
description	The paucity of microbiome studies at intestinal tissues has contributed to a yet limited understanding of potential viral and bacterial cofactors of colorectal cancer (CRC) carcinogenesis or progression. We analysed whole‐genome sequences of CRC primary tumours, their corresponding metastases and matched normal tissue for sequences of viral, phage and bacterial species. Bacteriome analysis showed Fusobacterium nucleatum, Streptococcus sanguinis, F. Hwasookii, Anaerococcus mediterraneensis and further species enriched in primary CRCs. The primary CRC of one patient was enriched for F. alocis, S. anginosus, Parvimonas micra and Gemella sp. 948. Enrichment of Escherichia coli strains IAI1, SE11, K‐12 and M8 was observed in metastases together with coliphages enterobacteria phage φ80 and Escherichia phage VT2φ_272. Virome analysis showed that phages were the most preponderant viral species (46%), the main families being Myoviridae, Siphoviridae and Podoviridae. Primary CRCs were enriched for bacteriophages, showing five phages (Enterobacteria, Bacillus, Proteus, Streptococcus phages) together with their pathogenic hosts in contrast to normal tissues. The most frequently detected, and Blast‐confirmed, viruses included human endogenous retrovirus K113, human herpesviruses 7 and 6B, Megavirus chilensis, cytomegalovirus (CMV) and Epstein–Barr virus (EBV), with one patient showing EBV enrichment in primary tumour and metastases. EBV was PCR‐validated in 80 pairs of CRC primary tumour and their corresponding normal tissues; in 21 of these pairs (26.3%), it was detectable in primary tumours only. The number of viral species was increased and bacterial species decreased in CRCs compared with normal tissues, and we could discriminate primary CRCs from metastases and normal tissues by applying the Hutcheson t‐test on the Shannon indices based on viral and bacterial species. Taken together, our results descriptively support hypotheses on microorganisms as potential (co)risk factors of CRC and extend putative suggestions on critical microbiome species in CRC metastasis.
format	article
author	Luigi Marongiu Jonathan J. M. Landry Tobias Rausch Mohammed L. Abba Susanne Delecluse Henri‐Jacques Delecluse Heike Allgayer
author_facet	Luigi Marongiu Jonathan J. M. Landry Tobias Rausch Mohammed L. Abba Susanne Delecluse Henri‐Jacques Delecluse Heike Allgayer
author_sort	Luigi Marongiu
title	Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
title_short	Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
title_full	Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
title_fullStr	Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
title_full_unstemmed	Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
title_sort	metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors
publisher	Wiley
publishDate	2021
url	https://doaj.org/article/7de803998014476aa150c199a99be616
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Metagenomic analysis of primary colorectal carcinomas and their metastases identifies potential microbial risk factors

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