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Genomic Insights Into the Acidobacteria Reveal Strategies for Their Success in Terrestrial Environments

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Genomic Insights Into the Acidobacteria Reveal Strategies for Their Success in Terrestrial Environments Environmental Microbiology (2018) 20(3), 1041–1063 doi:10.1111/1462-2920.14043 Genomic insights into the Acidobacteria reveal strategies for their success in terrestrial environments Stephanie A. Eichorst ,1*† Daniela Trojan ,1† acidobacteria genome analysis reveal traits that Simon Roux ,2 Craig Herbold ,1 provide genomic, physiological and metabolic versa- Thomas Rattei ,3 and Dagmar Woebken ,1 tility, presumably allowing flexibility and versatility in 1Division of Microbial Ecology, Department of the challenging and fluctuating soil environment. Microbiology and Ecosystem Science, Research Network “ Chemistry Meets Biology”, University of Vienna, Vienna, Austria. Introduction 2 Department of Energy, Joint Genome Institute, Walnut The phylum Acidobacteria constitute an abundant and Creek, CA, USA. ubiquitous bacterial phylum typically found in soils and 3Division of Computational Systems Biology, sediments. The widespread nature across members of this Department of Microbiology and Ecosystem Science, phylum in soils is clear; they have been detected in agricul- Research Network “ Chemistry Meets Biology”, tural soils (Navarrete et al., 2013), forest soils (Stursov a University of Vienna, Vienna, Austria. et al., 2012), peat soils (Pankratov, 2012), arctic tundra soils (Mannist€ o€ et al., 2012a), desert soils (Kuske et al., 1997; Dunbar et al., 2002) and across many edaphically Summary (defined here as of or relating to soil) diverse temperate Members of the phylum Acidobacteria are abundant soils (Jones et al., 2009). Not only are they ubiquitous, and ubiquitous across soils. We performed a large- they also have a high relative abundance based on rRNA scale comparative genome analysis spanning subdi- gene libraries (as high as 40% (range ca. 20%–40%) visions 1, 3, 4, 6, 8 and 23 (n 5 24) with the goal to (Lipson and S. K. Schmidt, 2004; Janssen, 2006) and identify features to help explain their prevalence in have a breadth of phylogenetic diversity similar to that of soils and understand their ecophysiology. Our analy- the Proteobacteria (Hugenholtz et al., 1998) spanning 26 sis revealed that bacteriophage integration events subdivisions known to date (Barns et al., 2007). along with transposable and mobile elements influ- Based on previous genomic and physiological investiga- enced the structure and plasticity of these genomes. tions, many subdivision 1 and 3 strains have been Low- and high-affinity respiratory oxygen reductases described as versatile heterotrophs that grow optimally at were detected in multiple genomes, suggesting the low pH, produce copious amounts of extracellular material, capacity for growing across different oxygen gra- harbour a low rRNA operon copy number suggesting an dients. Among many genomes, the capacity to use a oligotrophic (more K-selected) lifestyle, and contain both diverse collection of carbohydrates, as well as inor- low-specificity major facilitator superfamily and high-affinity ganic and organic nitrogen sources (such as via ABC-type transporters (Ward et al., 2009; Rawat et al., extracellular peptidases), was detected – both advan- 2012; Kielak et al., 2016). Some more striking physiologies such as iron reduction and/or fermentative growth (Liesack tageous traits in environments with fluctuating et al., 1994; Coates et al., 1999), phototrophy (Garcia nutrient environments. We also identified multiple Costas et al., 2012), along with the ability to grow under soil acidobacteria with the potential to scavenge thermophilic conditions have been described in select atmospheric concentrations of H , now encompass- 2 strains from subdivision 4, 8, 10 and 23 (Izumi et al., 2012; ing mesophilic soil strains within the subdivision 1 Losey et al., 2013; Crowe et al., 2014; Stamps et al., 2014; and 3, in addition to a previously identified thermo- Tank and Bryant, 2015a). Yet the vast majority of acidobac- philic strain in subdivision 4. This large-scale teria detected in soils based on culture dependent and independent approaches are members of subdivisions 1, Received 19 May, 2017; revised 16 December, 2017; accepted 2, 3, 4, 5 and 6 (Janssen, 2006; Jones et al., 2009). Many 8 January, 2018. *For correspondence. E-mail: eichorst@microbial- ecology.net; Tel. 143 1 4277 76610; Fax 143 1 4277 876613. strains in culture collections stem from these aforemen- †These authors contributed equally to the work. tioned ubiquitous subdivisions and were originally isolated VC 2018 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 1042 S. A. Eichorst et al. from soil environments such as tundra soils (Mannist€ o€ the number of genes detected in the genome was not dis- et al., 2012a), peatland soil (Pankratov et al., 2012; proportionately high. This indicates a low level of Dedysh et al., 2012), agricultural soil or meadow grassland population diversity rather than the presence of a contami- soil (Eichorst et al., 2007; Eichorst and Kuske, 2012; nating organism and is not expected to affect Foesel et al., 2013), forest soils (Koch et al., 2008; Llado phylogenomic and/or comparative analyses. The phyloge- et al., 2016) and subtropical soil (Huber et al., 2016). nomic tree, based on 43 concatenated universally Therefore, it is particularly pertinent to better understand conserved marker genes, depicted a similar subdivision these environmentally relevant soil strains. topology to the 16S rRNA gene tree, namely with clear dis- To that end, we sought to elucidate the potential eco- tinctions across subdivisions 1, 3, 4, 6, 8 and 23 (Fig. 2, physiology of the soil acidobacteria by undertaking a large- Fig. S1). Based on the phylogenomic tree, the phylum scale comparative acidobacterial genomic investigation Acidobacteria branches as a sister clade to the Aminice- comprising 24 genomes. Previous comparative genomic nantes (formerly Candidate division OP8) (Supporting investigations on acidobacteria coupled with physiological- Information Fig. S1). Aminicenantes have been found in based investigations have been limited to either three or hydrocarbon-impacted environments, marine habitats, six strains and have generated tremendous insights into aquatic, groundwater samples and terrestrial springs, typi- their physiology (Ward et al., 2009; Rawat et al., 2012). cally having a higher relative abundance in environments The expansion of published genomes in the databases characterized by low O2 concentrations, high temperatures along with novel genomes from this study demanded an and moderate to high salinity (Farag et al., 2014). updated investigation, with a focus on the features in the Subdivision 1 has the best representation in the phyloge- genomes that could help explain their ubiquity and abun- nomic tree with 15 genomes (Fig. 2). Within this subdivision, dance in soil. More specifically, we investigated (i) if there there is one main grouping consisting of three lineages: (i) are (any) systematic differences in gene content among Silvibacterium and Acidobacterium;(ii)Terracidiphilus and these ‘subdivision’ classifications and/or environments (iii) Terr iglobus, Granulicella and Edaphobacter.There from which the strains were isolated, (ii) events that appears to be a major split with ‘Candidatus Koribacter ver- shaped the genome structure of the strains, (iii) the genes satilis’ Ellin345, as it is distinct from these lineages. The that comprise the acidobacterial pan genome and (iv) what branching order of the phylogenomic tree relative to the 16S potential physiological features could allow for their ubiq- rRNA gene tree is fairly consistent with the exception of Ter- uity and prevalence across many soil environments. racidiphilus, which based on the 16S rRNA gene clusters with Silvibacterium and Acidobacterium (Supporting Infor- Results and discussion mation Fig. S1). Genomes stemming from the genus Terr iglobus exhibited a monophyletic grouping consisting of Phylogeny of investigated acidobacterial strains Terriglobus saanensis SP1PR4, T. roseus KBS 63 and Terri- The genomes investigated in this study along with the globus sp. TAA 43, and were most similar to a grouping references and abbreviations used can be found in Sup- consisting of Granulicella and Edaphobacter genomes. porting Information Table S1. The general genome Interestingly, the two species in the Granulicella genus did features of the new strains from this study are summarized not have a monophyletic nature based on the phylogenomic in Supporting Information Table S2 and described in more analysis, but formed a larger grouping with Acidobacteria- detail in (Trojan et al., in preparation). Briefly, the genome ceae bacteria KBS 89, TAA 166 and KBS 146 along with sizes of the new strains ranged from 4.9 to 6.7 Mb with a Edaphobacter aggregans DSM19364. A similar pattern was genome GC content of 57%–60%. The number of esti- observed in the 16S rRNA gene tree (Supporting Informa- mated protein coding sequences (CDS) with predicted tion Fig. S1). The other noted monophyletic genus cluster in function ranged from 68% to 76%. Based on the 16S subdivision 1 was the Acidobacterium genus, which encom- rRNA gene, the investigated genomes spanned subdivi- passed Acidobacterium capsulatum ATCC51196 and sions 1, 3, 4, 6, 8 and 23 (Fig. 1). There were at least two Acidobacterium ailaaui PMMR2
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