Geology and climate influence rhizobiome composition of the phenotypically diverse tropical tree Tabebuia heterophylla

diversity declined as the temperatures became more extreme. However, our data found pH was a strong diversity-driving factor, which is consistent with other studies [43–45], and mean annual precipitation also appears to be a key driver of microbial communities found across the different sites. The rhizosphere is a thin layer of soil surrounding the plant root, influenced by the root and its associated microbiota [8–10]. Plants produce an array of different exudates (e.g. amino acids, organic acids, polysaccharides) used by bacteria and archaea to produce energy [8, 10]. Thus, the rhizosphere will be dominated by microbes with the metabolic capacity to degrade those compounds in addition to other structural compounds such as lignin, commonly found within the plant litter [46, 47]. These degradation processes are essential for plant nutrient cycling, [48] biogeochemical cycles (e.g. nitrogen, phosphorus, calcium) and water uptake [49]. Several groups of microbes are known to alter the plant response to the environment [3], such as mycorrhizal fungi, nitrogen-fixing bacteria, and plant growth-promoting bacteria (PGPB). These groups alter the rhizosphere processes, which in turn regulate different aspects of nutrient cycling and water uptake, promoting the establishment of plants in stressed envi- ronments [3, 16]. Our study found a higher diversity of Verrucomicrobial OTUs in Volcanic sites, taxa well known to be glycosyl hydrolase rich heterotrophs, adapted to the utilization of sulfated glycopolymers such as those from subdivision 3 and soil clone MC18 [50]. Serpentine

sites are known to be nutrient-poor and high in heavy metals such as chromium, nickel, and cobalt [51]. We found locally adapted serpentine microorganisms in the rhizosphere of plants corresponding to dominance of Cyanobacteria such as Microcoleus and Phormidiaceae OTUs. Cyanobacteria have been shown to be able to tolerate the toxicity of heavy metals. Heavy met- als are well known to cause generation of reactive oxygen species (ROS) and reactive nitrogen species (NO) which are involved in the free radical chain reaction of membrane lipids and pro- teins [52]. Metal homeostasis is a special property of Cyanobacteria, as the photosynthetic machinery demands metals that act as cofactors of several proteins and other types of photo- synthetic metabolism [53]. Additionally, the adaptation to metal concentrations in Cyanobac- teria includes their ability to excrete heavy metal siderophores [54], the production of metalloproteins and metal transporters [55] and tolerance of a significant concentration of heavy metals by reducing the toxic effect of ROS with several antioxidant enzymes [53, 56]. Along with these, Chloracidobacterial OTUs were also found in high abundance in serpentine sites, which are also photosynthetic [57]. In the karst bedrock sites -known to be porous with underground drainage systems due to the rainfall–loss of nitrogen is common [58]. We found a higher abundance of Rhizobium, Rhodocyclales, Rhodospirillaceae and CCM11b OTUs in both karst sites in high abundance among all other genera and also in higher abundance com-

pared to the other volcanic and serpentine sites. These taxa are anoxygenic photoheterotrophs; plant-associated nitrogen-fixing aerobes, and non-sulfur photosynthetic bacteria [59]. Despite growing in stressful heavy-metal rich serpentine soils, Tabebuia trees select for ser- pentine tolerant bacteria and show a similar phenotype as nutrient-rich volcanic-adapted trees. Karst-adapted trees, especially those in very dry and hot climates, have the most distinct phenotype, although with a similar microbial diversity index and different microbial composi- tion; thus this extreme phenotype may well be a result of adaptation to aridity [60]. Our results suggest that climate and geology impact the rhizosphere microbial pool with consequences for their function and to the plant phenotype. Tabebuia microbiomes thus can indirectly improve the plant’s fitness (e.g. nutrient availability), which may ultimately result in an altered phenotype. PLOS ONE Rhizobiota of the tropical tree Tabebuia heterophylla PLOS ONE | https://doi.org/10.1371/journal.pone.0231083 April 7, 2020 12 / 16