Linking ecology and systematics of acidobacteria: Distinct habitat preferences of the Acidobacteriia and Blastocatellia in tundra soils

PLOS ONE RESEARCH ARTICLE Linking ecology and systematics of acidobacteria: Distinct habitat preferences of the Acidobacteriia and Blastocatellia in tundra soils Anastasia A. Ivanova1, Alena D. Zhelezova2, Timofey I. Chernov2, Svetlana N. Dedysh ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia, 2 Department of Soil Biology and Biochemistry, V.V. Dokuchaev Soil Science Institute, Moscow, Russia * Abstract OPEN ACCESS Citation: Ivanova AA, Zhelezova AD, Chernov TI, Dedysh SN (2020) Linking ecology and systematics of acidobacteria: Distinct habitat preferences of the Acidobacteriia and Blastocatellia in tundra soils. PLoS ONE 15(3): e0230157. https://doi.org/10.1371/journal.pone.0230157 Editor: Ying Ma, Universidade de Coimbra, PORTUGAL Received: August 20, 2019 Accepted: February 22, 2020 Published: March 17, 2020 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0230157 Copyright: © 2020 Ivanova et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The 16S rRNA gene sequence dataset used in this study is deposited with GenBank under the Bioproject accession number PRJNA497067 and is publicly available. The Acidobacteria is one of the major bacterial phyla in soils and peatlands. The currently explored diversity within this phylum is assigned to 15 class-level units, five of which contain described members. The ecologically relevant traits of acidobacteria from different classes remain poorly understood. Here, we compared the patterns of acidobacterial diversity in sandy soils of tundra, along a gradient of increasing vegetation–unfixed aeolian sand, semifixed surfaces with mosses and lichens, and mature soil under fully developed plant cover. The Acidobacteria-affiliated 16S rRNA gene sequences retrieved from these soils comprised 11 to 33% of total bacterial reads and belonged mostly to members of the classes Acidobacteriia and Blastocatellia, which displayed opposite habitat preferences. The relative abundance of the Blastocatellia was maximal in unfixed sands and declined in soils of vegetated plots, showing positive correlation with soil pH and negative correlation with carbon and nitrogen availability. An opposite tendency was characteristic for the Acidobacteriia. Most Blastocatellia-affiliated reads belonged to as-yet-undescribed members of the family Arenimicrobiaceae, which appears to be characteristic for dry, depleted in organic matter soil habitats. The pool of Acidobacteriia-affiliated sequences, apart from Acidobacteriaceaeand Bryobacteraceae-related reads, had a large proportion of sequences from as-yet-undescribed families, which seem to specialize in degrading plant-derived organic matter. This analysis reveals sandy soils of tundra as a source of novel acidobacterial diversity and provides an insight into the ecological preferences of different taxonomic groups within this phylum. Introduction The Acidobacteria is one of the most abundant and highly diverse bacterial phyla in soils and peatlands [1–6]. The proportion of Acidobacteria-affiliated 16S rRNA gene reads in sequence PLOS ONE | https://doi.org/10.1371/journal.pone.0230157 March 17, 2020 1 / 19 PLOS ONE Funding: This study was supported by the Russian Science Foundation (RSF -http://www.rscf.ru/en/ Field studies and 16S rRNA gene sequencing were performed by A.Z. and T.C. and supported by the project No 17-16-01057. Bioinformatic and taxonomic analyses were performed by A.I. and S. D. and were supported by the project No 16-1410210. The funder had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Habitat preferences of the Acidobacteria in tundra soils pools retrieved from various soil habitats ranges between 5 and 50% of the total bacterial community [3,7–10]. Our knowledge of the roles of acidobacteria in soils includes decomposition of various biopolymers and participation in the global cycling of carbon, iron and hydrogen, but this list of functional capabilities remains far from being complete and is attributed to several sub-groups of this phylum only. The currently explored diversity within the Acidobacteria is commonly addressed as corresponding to 26 major 16S rRNA gene sequence clades or subdivisions (SD) [11]. Recently, these 26 subdivisions were assigned to 15 class-level units, five of which contain described members [12]. These include three earlier established classes Acidobacteriia, Blastocatellia and Holophagae [13–15] as well as two recently proposed classes Vicinamibacteria and Thermoanaerobaculia [12]. The phylogenetic range of the class Acidobacteriia accommodates 16S rRNA gene sequences from several SDs including 1, 2, 3, 5, 11, 12, 13, 14, 15, and 24. The classes Blastocatellia, Vicinamibacteria and Thermoanaerobaculia correspond to one subdivision each, i.e. SDs 4, 6, and 23, while the class Holophagae includes SDs 8 and 22. In soil, acidobacterial SDs 1, 2, 3, 4 and 6 are the most abundant ones [8]. This is true for a wide range of ecosystem types, including boreal and tropical forests, grasslands and pastures, as well as arid landscapes [3–5, 8–10]. The abundances of subdivisions 1, 2 and 3 show negative correlation with soil pH, while the opposite tendency is characteristic for subdivisions 4 and 6 [8]. Peatlands are also among the preferred habitats of Acidobacteria. Acidic Sphagnum-dominated boreal peatlands are colonized mainly by members of SDs 1 and 3 [16–18]. Subarctic peatlands, in addition to SDs 1 and 3, may contain a relatively high proportion of SD2 Acidobacteria [19,20]. Despite their wide distribution in various soils, acidobacteria remain strongly underrepresented in culture collections due to difficulties in their cultivation and laboratory maintenance [6]. Much of the currently described diversity (ca. 15 genera) belong to the class Acidobacteriia, which includes the orders Acidobacteriales and Bryobacterales (SDs 1 and 3), and accommodates acidophilic or acidotolerant, mesophilic and psychrotolerant, chemoheterotrophic bacteria that utilize various sugars and polysaccharides and possess a number of hydrolytic capabilities [12]. The class Blastocatellia contains 7 genera of aerobic, mesophilic or thermophilic, chemo-heterotrophic bacteria that specialize on degradation of complex pr (...truncated)