Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems

ABSTRACT Marine and freshwater microbial communities are phylogenetically distinct, and transitions between habitat types are thought to be infrequent. We compared the phylogenetic diversity of marine and freshwater microorganisms and identified specific lineages exhibiting notably high or low simil...

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Autores principales:	Sara F. Paver, Daniel Muratore, Ryan J. Newton, Maureen L. Coleman
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	16S rRNA SAR11 aquatic ecology aquatic microbiology biogeography environmental transitions Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/313968515c3043f1a1068e7966a02667
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spelling	oai:doaj.org-article:313968515c3043f1a1068e7966a026672021-12-02T19:47:34ZReevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems10.1128/mSystems.00232-182379-5077https://doaj.org/article/313968515c3043f1a1068e7966a026672018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00232-18https://doaj.org/toc/2379-5077ABSTRACT Marine and freshwater microbial communities are phylogenetically distinct, and transitions between habitat types are thought to be infrequent. We compared the phylogenetic diversity of marine and freshwater microorganisms and identified specific lineages exhibiting notably high or low similarity between marine and freshwater ecosystems using a meta-analysis of 16S rRNA gene tag-sequencing data sets. As expected, marine and freshwater microbial communities differed in the relative abundance of major phyla and contained habitat-specific lineages. At the same time, and contrary to expectations, many shared taxa were observed in both habitats. Based on several metrics, we found that Gammaproteobacteria, Alphaproteobacteria, Bacteroidetes, and Betaproteobacteria contained the highest number of closely related marine and freshwater sequences, suggesting comparatively recent habitat transitions in these groups. Using the abundant alphaproteobacterial group SAR11 as an example, we found evidence that new lineages, beyond the recognized LD12 clade, are detected in freshwater at low but reproducible abundances; this evidence extends beyond the 16S rRNA locus to core genes throughout the genome. Our results suggest that shared taxa are numerous, but tend to occur sporadically and at low relative abundance in one habitat type, leading to an underestimation of transition frequency between marine and freshwater habitats. Rare taxa with abundances near or below detection, including lineages that appear to have crossed the salty divide relatively recently, may possess adaptations enabling them to exploit opportunities for niche expansion when environments are disturbed or conditions change. IMPORTANCE The distribution of microbial diversity across environments yields insight into processes that create and maintain this diversity as well as potential to infer how communities will respond to future environmental changes. We integrated data sets from dozens of freshwater lake and marine samples to compare diversity across open water habitats differing in salinity. Our novel combination of sequence-based approaches revealed lineages that likely experienced a recent transition across habitat types. These taxa are promising targets for studying physiological constraints on salinity tolerance. Our findings contribute to understanding the ecological and evolutionary controls on microbial distributions, and open up new questions regarding the plasticity and adaptability of particular lineages.Sara F. PaverDaniel MuratoreRyan J. NewtonMaureen L. ColemanAmerican Society for Microbiologyarticle16S rRNASAR11aquatic ecologyaquatic microbiologybiogeographyenvironmental transitionsMicrobiologyQR1-502ENmSystems, Vol 3, Iss 6 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	16S rRNA SAR11 aquatic ecology aquatic microbiology biogeography environmental transitions Microbiology QR1-502
spellingShingle	16S rRNA SAR11 aquatic ecology aquatic microbiology biogeography environmental transitions Microbiology QR1-502 Sara F. Paver Daniel Muratore Ryan J. Newton Maureen L. Coleman Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
description	ABSTRACT Marine and freshwater microbial communities are phylogenetically distinct, and transitions between habitat types are thought to be infrequent. We compared the phylogenetic diversity of marine and freshwater microorganisms and identified specific lineages exhibiting notably high or low similarity between marine and freshwater ecosystems using a meta-analysis of 16S rRNA gene tag-sequencing data sets. As expected, marine and freshwater microbial communities differed in the relative abundance of major phyla and contained habitat-specific lineages. At the same time, and contrary to expectations, many shared taxa were observed in both habitats. Based on several metrics, we found that Gammaproteobacteria, Alphaproteobacteria, Bacteroidetes, and Betaproteobacteria contained the highest number of closely related marine and freshwater sequences, suggesting comparatively recent habitat transitions in these groups. Using the abundant alphaproteobacterial group SAR11 as an example, we found evidence that new lineages, beyond the recognized LD12 clade, are detected in freshwater at low but reproducible abundances; this evidence extends beyond the 16S rRNA locus to core genes throughout the genome. Our results suggest that shared taxa are numerous, but tend to occur sporadically and at low relative abundance in one habitat type, leading to an underestimation of transition frequency between marine and freshwater habitats. Rare taxa with abundances near or below detection, including lineages that appear to have crossed the salty divide relatively recently, may possess adaptations enabling them to exploit opportunities for niche expansion when environments are disturbed or conditions change. IMPORTANCE The distribution of microbial diversity across environments yields insight into processes that create and maintain this diversity as well as potential to infer how communities will respond to future environmental changes. We integrated data sets from dozens of freshwater lake and marine samples to compare diversity across open water habitats differing in salinity. Our novel combination of sequence-based approaches revealed lineages that likely experienced a recent transition across habitat types. These taxa are promising targets for studying physiological constraints on salinity tolerance. Our findings contribute to understanding the ecological and evolutionary controls on microbial distributions, and open up new questions regarding the plasticity and adaptability of particular lineages.
format	article
author	Sara F. Paver Daniel Muratore Ryan J. Newton Maureen L. Coleman
author_facet	Sara F. Paver Daniel Muratore Ryan J. Newton Maureen L. Coleman
author_sort	Sara F. Paver
title	Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
title_short	Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
title_full	Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
title_fullStr	Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
title_full_unstemmed	Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems
title_sort	reevaluating the salty divide: phylogenetic specificity of transitions between marine and freshwater systems
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/313968515c3043f1a1068e7966a02667
work_keys_str_mv	AT sarafpaver reevaluatingthesaltydividephylogeneticspecificityoftransitionsbetweenmarineandfreshwatersystems AT danielmuratore reevaluatingthesaltydividephylogeneticspecificityoftransitionsbetweenmarineandfreshwatersystems AT ryanjnewton reevaluatingthesaltydividephylogeneticspecificityoftransitionsbetweenmarineandfreshwatersystems AT maureenlcoleman reevaluatingthesaltydividephylogeneticspecificityoftransitionsbetweenmarineandfreshwatersystems
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Reevaluating the Salty Divide: Phylogenetic Specificity of Transitions between Marine and Freshwater Systems

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