Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust

ABSTRACT Biological soil crusts (biocrusts) are photosynthetic “hot spots” in deserts and cover ∼12% of the Earth’s terrestrial surface, and yet they face an uncertain future given expected shifts in rainfall events. Laboratory wetting of biocrust communities is known to cause a bloom of Firmicutes...

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Autores principales:	Marc W. Van Goethem, Tami L. Swenson, Gareth Trubl, Simon Roux, Trent R. Northen
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Firmicutes bacteriophages biocrust soil microbiology virus-host interactions wetting Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/103183ef07294aaa84d4e573f8f8e1ee
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spelling	oai:doaj.org-article:103183ef07294aaa84d4e573f8f8e1ee2021-11-15T15:54:47ZCharacteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust10.1128/mBio.02287-192150-7511https://doaj.org/article/103183ef07294aaa84d4e573f8f8e1ee2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02287-19https://doaj.org/toc/2150-7511ABSTRACT Biological soil crusts (biocrusts) are photosynthetic “hot spots” in deserts and cover ∼12% of the Earth’s terrestrial surface, and yet they face an uncertain future given expected shifts in rainfall events. Laboratory wetting of biocrust communities is known to cause a bloom of Firmicutes which rapidly become dominant community members within 2 days after emerging from a sporulated state. We hypothesized that their bacteriophages (phages) would respond to such a dramatic increase in their host’s abundance. In our experiment, wetting caused Firmicutes to bloom and triggered a significant depletion of cyanobacterial diversity. We used genome-resolved metagenomics to link phage to their hosts and found that the bloom of the genus Bacillus correlated with a dramatic increase in the number of Caudovirales phages targeting these diverse spore-formers (r = 0.762). After 2 days, we observed dramatic reductions in the relative abundances of Bacillus, while the number of Bacillus phages continued to increase, suggestive of a predator-prey relationship. We found predicted auxiliary metabolic genes (AMGs) associated with sporulation in several Caudovirales genomes, suggesting that phages may influence and even benefit from sporulation dynamics in biocrusts. Prophage elements and CRISPR-Cas repeats in Firmicutes metagenome-assembled genomes (MAGs) provide evidence of recent infection events by phages, which were corroborated by mapping viral contigs to their host MAGs. Combined, these findings suggest that the blooming Firmicutes become primary targets for biocrust Caudovirales phages, consistent with the classical “kill-the-winner” hypothesis. IMPORTANCE This work forms part of an overarching research theme studying the effects of a changing climate on biological soil crust (biocrust) in the Southwestern United States. To our knowledge, this study was the first to characterize bacteriophages in biocrust and offers a view into the ecology of phages in response to a laboratory wetting experiment. The phages identified here represent lineages of Caudovirales, and we found that the dynamics of their interactions with their Firmicutes hosts explain the collapse of a bacterial bloom that was induced by wetting. Moreover, we show that phages carried host-altering metabolic genes and found evidence of proviral infection and CRISPR-Cas repeats within host genomes. Our results suggest that phages exert controls on population density by lysing dominant bacterial hosts and that they further impact biocrust by acquiring host genes for sporulation. Future research should explore how dominant these phages are in other biocrust communities and quantify how much the control and lysis of blooming populations contributes to nutrient cycling in biocrusts.Marc W. Van GoethemTami L. SwensonGareth TrublSimon RouxTrent R. NorthenAmerican Society for MicrobiologyarticleFirmicutesbacteriophagesbiocrustsoil microbiologyvirus-host interactionswettingMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Firmicutes bacteriophages biocrust soil microbiology virus-host interactions wetting Microbiology QR1-502
spellingShingle	Firmicutes bacteriophages biocrust soil microbiology virus-host interactions wetting Microbiology QR1-502 Marc W. Van Goethem Tami L. Swenson Gareth Trubl Simon Roux Trent R. Northen Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
description	ABSTRACT Biological soil crusts (biocrusts) are photosynthetic “hot spots” in deserts and cover ∼12% of the Earth’s terrestrial surface, and yet they face an uncertain future given expected shifts in rainfall events. Laboratory wetting of biocrust communities is known to cause a bloom of Firmicutes which rapidly become dominant community members within 2 days after emerging from a sporulated state. We hypothesized that their bacteriophages (phages) would respond to such a dramatic increase in their host’s abundance. In our experiment, wetting caused Firmicutes to bloom and triggered a significant depletion of cyanobacterial diversity. We used genome-resolved metagenomics to link phage to their hosts and found that the bloom of the genus Bacillus correlated with a dramatic increase in the number of Caudovirales phages targeting these diverse spore-formers (r = 0.762). After 2 days, we observed dramatic reductions in the relative abundances of Bacillus, while the number of Bacillus phages continued to increase, suggestive of a predator-prey relationship. We found predicted auxiliary metabolic genes (AMGs) associated with sporulation in several Caudovirales genomes, suggesting that phages may influence and even benefit from sporulation dynamics in biocrusts. Prophage elements and CRISPR-Cas repeats in Firmicutes metagenome-assembled genomes (MAGs) provide evidence of recent infection events by phages, which were corroborated by mapping viral contigs to their host MAGs. Combined, these findings suggest that the blooming Firmicutes become primary targets for biocrust Caudovirales phages, consistent with the classical “kill-the-winner” hypothesis. IMPORTANCE This work forms part of an overarching research theme studying the effects of a changing climate on biological soil crust (biocrust) in the Southwestern United States. To our knowledge, this study was the first to characterize bacteriophages in biocrust and offers a view into the ecology of phages in response to a laboratory wetting experiment. The phages identified here represent lineages of Caudovirales, and we found that the dynamics of their interactions with their Firmicutes hosts explain the collapse of a bacterial bloom that was induced by wetting. Moreover, we show that phages carried host-altering metabolic genes and found evidence of proviral infection and CRISPR-Cas repeats within host genomes. Our results suggest that phages exert controls on population density by lysing dominant bacterial hosts and that they further impact biocrust by acquiring host genes for sporulation. Future research should explore how dominant these phages are in other biocrust communities and quantify how much the control and lysis of blooming populations contributes to nutrient cycling in biocrusts.
format	article
author	Marc W. Van Goethem Tami L. Swenson Gareth Trubl Simon Roux Trent R. Northen
author_facet	Marc W. Van Goethem Tami L. Swenson Gareth Trubl Simon Roux Trent R. Northen
author_sort	Marc W. Van Goethem
title	Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
title_short	Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
title_full	Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
title_fullStr	Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
title_full_unstemmed	Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust
title_sort	characteristics of wetting-induced bacteriophage blooms in biological soil crust
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/103183ef07294aaa84d4e573f8f8e1ee
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Characteristics of Wetting-Induced Bacteriophage Blooms in Biological Soil Crust

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