Adaptation of Microbial Communities to Environmental Arsenic and Selection of Arsenite-Oxidizing Bacteria From Contaminated Groundwaters

Abstract

Arsenic mobilization in groundwater systems is driven by a variety of functionally diverse microorganisms and complex interconnections between different physicochemical factors. In order to unravel this great ecosystem complexity, groundwaters with varying background concentrations and speciation of arsenic were considered in the Po Plain (Northern Italy), one of the most populated areas in Europe affected by metalloid contamination. High-throughput Illumina 16S rRNA gene sequencing, CARD-FISH and enrichment of arsenic-transforming consortia showed that among the analyzed groundwaters, diverse microbial communities were present, both in terms of diversity and functionality. Oxidized inorganic arsenic [arsenite, As(III)] was the main driver that shaped each community. Several uncharacterized members of the genus Pseudomonas, putatively involved in metalloid transformation, were revealed in situ in the most contaminated samples. With a cultivation approach, arsenic metabolisms potentially active at the site were evidenced. In chemolithoautotrophic conditions, As(III) oxidation rate linearly correlated to As(III) concentration measured at the parental sites, suggesting that local As(III) concentration was a relevant factor that selected for As(III)-oxidizing bacterial populations. In view of the exploitation of these As(III)-oxidizing consortia in biotechnology-based arsenic bioremediation actions, these results suggest that contaminated aquifers in Northern Italy host unexplored microbial populations that provide essential ecosystem services.

Local and global chemical shaping of bacterial communities by redox potential

“…4), among shallow and deep groundwater samples in Lower Chao Praya Basin (Sonthiphand et al, 2021b), and in the Po Plain, Northern Italy (Zecchin et al, 2021). Notably, arsenic was identified as a major driver of community structure in several of these studies (Sonthiphand et al, 2021a(Sonthiphand et al, , 2019Zecchin et al, 2021). A novel hypothesis to emerge from the present analysis is that arsenic contamination may interfere with the redox-based chemical shaping of the bacterial communities.…”

“…In contrast, there is a negative correlation between bacterial Z C and Eh7 for groundwater and surface water samples from the Golmud area in the Qaidam Basin, China (Guo et al, 2019), in the vicinity of a gold mine in Phetchabun and Pichit provinces in Thailand (Sonthiphand et al, 2021a) (Fig. 4), among shallow and deep groundwater samples in Lower Chao Praya Basin (Sonthiphand et al, 2021b), and in the Po Plain, Northern Italy (Zecchin et al, 2021). Notably, arsenic was identified as a major driver of community structure in several of these studies (Sonthiphand et al, 2021a(Sonthiphand et al, , 2019Zecchin et al, 2021).…”

“…Redox potential, abbreviated as Eh or ORP, is a measure of oxidizing power in a chemical system. Redox potential has been used as a monitor of microcosm development (Pagaling et al, 2014) and ecosystem health (Lanzén et al, 2021) and has important roles for assessing bioremediation (Li et al, 2021;Zecchin et al, 2021) and soil disinfestation (Poret-Peterson et al, 2020) strategies. Although measurements in natural systems generally reflect "mixed potentials" that have no clear thermodynamic interpretation (Bricker, 1982;Tan et al, 2017), the appearance of Eh in numerous microbial ecology studies calls for a better theoretical development of the ecological relevance of this parameter.…”

Influence of host genotype in establishing root associated microbiome of indica rice cultivars for plant growth promotion

“…Well-distributed populations of dissimilatory sulphate reducing taxa, such as Desulfobacteraceae , and Desulfobulbaceae were showing niche specificity to rice rhizosphere. This taxon has been found to switch from sulfate to nitrate respiration as an alternative respiratory metabolism under an abundance of nitrate ( Wörner et al, 2016 ; Zecchin et al, 2021 ). Dissimilatory nitrate reduction to ammonium (DNRA) is a characteristic of genera Paracocccus and Pseudoxanthomonas , which are reported from soil and groundwater sediments, and rhizosphere of corn, cotton, soya, and millet ( Mohapatra et al, 2018 ; Pan et al, 2020 ).…”

Occurrence, Geochemistry and Speciation of Elevated Arsenic Concentrations in a Fractured Bedrock Aquifer System

“…The pentavalent form of arsenic, arsenate (As V ) and the trivalent form, arsenite (As III ), are the most detected forms in groundwater (Zecchin et al 2021). Arsenate forms the oxyanions H 2 AsO 4 − and HAsO 4 − in oxidising environments in natural waters, while arsenite forms the oxyanions H 3 AsO 3 0 and H 2 AsO 3 − in reducing environments with the degree of protonation depending on pH (Garelick et al 2009;Herath et al 2016).…”