On the ecology ofAcinetobacter baumannii– jet stream rider and opportunist by nature
Authors: Wilharm Gottfried , Skiebe Evelyn , Łopińska Andżelina , Higgins Paul G. , Weber Kristin , Schaudinn Christoph , Neugebauer Christof , Görlitz Katharina , Meimers Gideon , Rizova Yana , Blaschke Ulrike , Heider Christine , Cuny Christiane , Drewes Stephan , Heuser Elisa , Jeske Kathrin , Jacob Jens , Ulrich Rainer G. , Bochenski Marcin , Kasprzak Mariusz , Burda Ewa , Ciepliński Mateusz , Kaługa Ireneusz , Jankowiak Łukasz , Aguirre José I. , López-García Alejandro , Höfle Ursula , Jagiello Zuzanna , Tobółka Marcin , Janic Bartosz , Zieliński Piotr , Kamiński Maciej , Frisch Johannes , Siekiera Joachim , Wendel Andreas F. , Brauner Paul , Jäckel Udo , Kaatz Michael , Müller Stefanie , Lübke-Becker Antina , Wieler Lothar H. , von Wachsmann Johanna , Thrukonda Lakshmipriya , Helal Mustafa , Epping Lennard , Wolf Silver A. , Semmler Torsten , Jerzak Leszek 
Published: January 2024

SummaryThe natural reservoirs of the nosocomial pathogenAcinetobacter baumanniiare not well defined. We previously identified white storks as a model system to study the ecology ofA. baumannii. Having screened more than 1,300 white stork nestlings over a period of six years across different regions of Poland and Germany (overall isolation rate of ∼29.5%), including food chain analyses and environmental samplings, we come up with a detailed picture of the dynamics and diversity ofA. baumanniiin their natural habitats. Adult storks, rather than being stably colonized with strains ofA. baumanniiwhich are successively transferred to their offspring, instead initially encounter these bacteria while foraging. Among their common food sources, consisting of earthworms, small mammals, and insects, we identified earthworms as a potential source ofA. baumannii, but more so the associated soil as well as plant roots. Through this, hotspot soil and compost habitats were identified which enable population dynamics to be studied over the course of the year. We demonstrate that sterilized plant material is rapidly colonized by airborneA. baumanniisuggesting they patrol to search for novel habitats, being opportunist by nature. The prevalence ofA. baumanniiexhibited a strong seasonality and peaked during summer. The strains we collected in Poland and Germany represent more than 50% of the worldwide known diversity in terms of the intrinsic OXA-51-like β-lactamase. A set of ∼400 genomes was determined and compared to a diverse set of publicly available genomes. Our pan-genome estimate of the species (∼51,000 unique genes) more than doubles the amount proposed by previous studies. Core-genome based phylogenetic analyses illustrated numerous links between wildlife isolates and hospital strains, including ancient as well as recent intercontinental transfer. Our data further suggest massive radiation within the species early after its emergence, matching with human activity during the Neolithic. Deforestation in particular seemed to set the stage for this bloom as we found that forests do not provide conducive conditions for the proliferation ofA. baumannii. In contrast, wet and nutrient-rich soil alongside rivers sampled during the summer can yield an isolation rate of ∼30%. Linking published work on the interaction betweenA. baumanniiand fungi and on aspergillosis as a major cause of mortality in white stork nestlings to our findings, we hypothesized that fungi andA. baumanniishare a long history of coevolution. Interaction studies revealed the capability ofA. baumanniito adhere to fungal spores and to suppress spore germination. Taken together, the intrinsic resistance endowment and potential to acquire antibiotic resistance can be explained by coevolution with antibiotic-producing fungi and other microorganisms within soil, and resistance to desiccation stress and radiation can be interpreted in the light of intercontinental hitchhiking through fungal spores.Originality - SignificanceThe ecology of the nosocomial pathogenAcinetobacter baumanniiremains poorly understood outside the hospital. Here, we present the most comprehensive study on its environmental biology to date, after having collected more than 1,450 independent isolates of which around 400 were whole genome-sequenced. This study more than doubles the size of the pan-genome of the species, illustrating both the diversity of our collection and the bias of previous work, but also the bottleneck for the establishment of lineages within the hospital environment. We reached isolation rates of about 30% both in white stork (Ciconia ciconia) nestlings and in soil samples when considering for sampling all preferences ofA. baumanniiwe uncovered. Thus, it is now possible to study the ecology and evolution ofA. baumanniiin nature at an unprecedented temporal and spatial resolution. We describe the worldwide spread ofA. baumanniilineages in nature as an ancient phenomenon that even surpasses that of human-associated bacteria in magnitude. This is likely due to airborne spread, putatively facilitated by association with fungal spores. We propose thatA. baumanniiis an opportunist by nature, using airborne patrolling to rapidly enter new suitable habitats consisting of organic matter in early stages of decomposition. Our collective data suggest thatA. baumannii, early after its speciation, went through massive radiation during the Neolithic, likely due to deforestation, settlement and farming producing numerous favorable habitats. Their natural lifestyle, which requires rapid adaptability to various habitats as well as tolerance to desiccation, radiation and antibiotic stress, perfectly predispose these opportunistic pathogens to establish within the hospital setting. Comparison of genomes from environmental and clinical isolates will now enable studies of the adaptive evolution of environmental bacteria towards multidrug-resistant opportunistic pathogens.