Verrucomicrobia are prevalent in north-temperate freshwater lakes and display class-level preferences between lake habitats

Edna Chiang; Marian L Schmidt; Michelle A Berry; Bopaiah A Biddanda; Ashley Burtner; Thomas H Johengen; Danna Palladino; Vincent J Denef

doi:10.1371/journal.pone.0195112

Verrucomicrobia are prevalent in north-temperate freshwater lakes and display class-level preferences between lake habitats

PLoS One. 2018 Mar 28;13(3):e0195112. doi: 10.1371/journal.pone.0195112. eCollection 2018.

Authors

Edna Chiang¹, Marian L Schmidt¹, Michelle A Berry¹, Bopaiah A Biddanda², Ashley Burtner³, Thomas H Johengen³, Danna Palladino³, Vincent J Denef¹

Affiliations

¹ Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, United States of America.
² Annis Water Resources Institute, Grand Valley State University, Muskegon, MI, United States of America.
³ Cooperative Institute for Great Lakes Research, University of Michigan, Ann Arbor, MI, United States of America.

Abstract

The bacterial phylum Verrucomicrobia was formally described two decades ago and originally believed to be a minor member of many ecosystems; however, it is now recognized as ubiquitous and abundant in both soil and aquatic systems. Nevertheless, knowledge of the drivers of its relative abundance and within-phylum habitat preferences remains sparse, especially in lake systems. Here, we documented the distribution of Verrucomicrobia in 12 inland lakes in Southeastern Michigan, a Laurentian Great Lake (Lake Michigan), and a freshwater estuary, which span a gradient in lake sizes, depths, residence times, and trophic states. A wide range of physical and geochemical parameters was covered by sampling seasonally from the surface and bottom of each lake, and by separating samples into particle-associated and free-living fractions. On average, Verrucomicrobia was the 4th most abundant phylum (range 1.7-41.7%). Fraction, season, station, and depth explained up to 70% of the variance in Verrucomicrobia community composition and preference for these habitats was phylogenetically conserved at the class-level. When relative abundance was linearly modeled against environmental data, Verrucomicrobia and non-Verrucomicrobia bacterial community composition correlated to similar quantitative environmental parameters, although there were lake system-dependent differences and > 55% of the variance remained unexplained. A majority of the phylum exhibited preference for the particle-associated fraction and two classes (Opitutae and Verrucomicrobiae) were identified to be more abundant during the spring season. This study highlights the high relative abundance of Verrucomicrobia in north temperate lake systems and expands insights into drivers of within-phylum habitat preferences of the Verrucomicrobia.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Aquatic Organisms / microbiology*
Biodiversity
Ecosystem*
Fresh Water / microbiology*
Lakes / microbiology*
Phylogeny
RNA, Ribosomal, 16S
Seasons
Verrucomicrobia / classification
Verrucomicrobia / physiology*
Water Microbiology*

Substances

RNA, Ribosomal, 16S

Grants and funding

This work was supported by the Fred A. and Barbara M. Erb Family Foundation through the University of Michigan Water Center (VJD, THJ); the Community Sequencing Program (U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported under Contract No. DE-AC02-05CH11231)(VJD); The NOAA Michigan Sea Grant (VJD); the National Science Foundation Graduate Research Fellowship Program (MLS); and scholarships from the American Society of Microbiology-Undergraduate Research Fellowship, the UM Honors Summer Fellowship, and the Beckman Scholars Program (EC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.