Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization

ABSTRACT Carbonate chimneys at the Lost City hydrothermal field are coated in biofilms dominated by a single phylotype of archaea known as Lost City Methanosarcinales. In this study, we have detected surprising physiological complexity in single-species biofilms, which is typically indicative of mul...

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Autores principales:	William J. Brazelton, Mausmi P. Mehta, Deborah S. Kelley, John A. Baross
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ee092a9b355147a8a559c023916704d5
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spelling	oai:doaj.org-article:ee092a9b355147a8a559c023916704d52021-11-15T15:38:45ZPhysiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization10.1128/mBio.00127-112150-7511https://doaj.org/article/ee092a9b355147a8a559c023916704d52011-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00127-11https://doaj.org/toc/2150-7511ABSTRACT Carbonate chimneys at the Lost City hydrothermal field are coated in biofilms dominated by a single phylotype of archaea known as Lost City Methanosarcinales. In this study, we have detected surprising physiological complexity in single-species biofilms, which is typically indicative of multispecies biofilm communities. Multiple cell morphologies were visible within the biofilms by transmission electron microscopy, and some cells contained intracellular membranes that may facilitate methane oxidation. Both methane production and oxidation were detected at 70 to 80°C and pH 9 to 10 in samples containing the single-species biofilms. Both processes were stimulated by the presence of hydrogen (H2), indicating that methane production and oxidation are part of a syntrophic interaction. Metagenomic data included a sequence encoding AMP-forming acetyl coenzyme A synthetase, indicating that acetate may play a role in the methane-cycling syntrophy. A wide range of nitrogen fixation genes were also identified, many of which were likely acquired via lateral gene transfer (LGT). Our results indicate that cells within these single-species biofilms may have differentiated into multiple physiological roles to form multicellular communities linked by metabolic interactions and LGT. Communities similar to these Lost City biofilms are likely to have existed early in the evolution of life, and we discuss how the multicellular characteristics of ancient hydrogen-fueled biofilm communities could have stimulated ecological diversification, as well as unity of biochemistry, during the earliest stages of cellular evolution. IMPORTANCE Our previous work at the Lost City hydrothermal field has shown that its carbonate chimneys host microbial biofilms dominated by a single uncultivated “species” of archaea. In this paper, we integrate evidence from these previous studies with new data on the metabolic activity and cellular morphology of these archaeal biofilms. We conclude that the archaeal biofilm must contain cells that are physiologically and possibly genetically differentiated with respect to each other. These results are especially interesting considering the possibility that the first cells originated and evolved in hydrothermal systems similar to Lost City.William J. BrazeltonMausmi P. MehtaDeborah S. KelleyJohn A. BarossAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 4 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 William J. Brazelton Mausmi P. Mehta Deborah S. Kelley John A. Baross Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
description	ABSTRACT Carbonate chimneys at the Lost City hydrothermal field are coated in biofilms dominated by a single phylotype of archaea known as Lost City Methanosarcinales. In this study, we have detected surprising physiological complexity in single-species biofilms, which is typically indicative of multispecies biofilm communities. Multiple cell morphologies were visible within the biofilms by transmission electron microscopy, and some cells contained intracellular membranes that may facilitate methane oxidation. Both methane production and oxidation were detected at 70 to 80°C and pH 9 to 10 in samples containing the single-species biofilms. Both processes were stimulated by the presence of hydrogen (H2), indicating that methane production and oxidation are part of a syntrophic interaction. Metagenomic data included a sequence encoding AMP-forming acetyl coenzyme A synthetase, indicating that acetate may play a role in the methane-cycling syntrophy. A wide range of nitrogen fixation genes were also identified, many of which were likely acquired via lateral gene transfer (LGT). Our results indicate that cells within these single-species biofilms may have differentiated into multiple physiological roles to form multicellular communities linked by metabolic interactions and LGT. Communities similar to these Lost City biofilms are likely to have existed early in the evolution of life, and we discuss how the multicellular characteristics of ancient hydrogen-fueled biofilm communities could have stimulated ecological diversification, as well as unity of biochemistry, during the earliest stages of cellular evolution. IMPORTANCE Our previous work at the Lost City hydrothermal field has shown that its carbonate chimneys host microbial biofilms dominated by a single uncultivated “species” of archaea. In this paper, we integrate evidence from these previous studies with new data on the metabolic activity and cellular morphology of these archaeal biofilms. We conclude that the archaeal biofilm must contain cells that are physiologically and possibly genetically differentiated with respect to each other. These results are especially interesting considering the possibility that the first cells originated and evolved in hydrothermal systems similar to Lost City.
format	article
author	William J. Brazelton Mausmi P. Mehta Deborah S. Kelley John A. Baross
author_facet	William J. Brazelton Mausmi P. Mehta Deborah S. Kelley John A. Baross
author_sort	William J. Brazelton
title	Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
title_short	Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
title_full	Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
title_fullStr	Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
title_full_unstemmed	Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization
title_sort	physiological differentiation within a single-species biofilm fueled by serpentinization
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/ee092a9b355147a8a559c023916704d5
work_keys_str_mv	AT williamjbrazelton physiologicaldifferentiationwithinasinglespeciesbiofilmfueledbyserpentinization AT mausmipmehta physiologicaldifferentiationwithinasinglespeciesbiofilmfueledbyserpentinization AT deborahskelley physiologicaldifferentiationwithinasinglespeciesbiofilmfueledbyserpentinization AT johnabaross physiologicaldifferentiationwithinasinglespeciesbiofilmfueledbyserpentinization
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Physiological Differentiation within a Single-Species Biofilm Fueled by Serpentinization

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