Stochasticity-driven weekly fluctuations distinguished the temporal pattern of particle-associated microorganisms from its free-living counterparts in temperate coastal seawater

Yulin Zhang; Jiwen Liu; Derui Song; Peng Yao; Shaodong Zhu; Yi Zhou; Jian Jin; Xiao-Hua Zhang

doi:10.1016/j.watres.2023.120849

Stochasticity-driven weekly fluctuations distinguished the temporal pattern of particle-associated microorganisms from its free-living counterparts in temperate coastal seawater

Water Res. 2024 Jan 1:248:120849. doi: 10.1016/j.watres.2023.120849. Epub 2023 Nov 8.

Authors

Yulin Zhang¹, Jiwen Liu², Derui Song¹, Peng Yao³, Shaodong Zhu¹, Yi Zhou¹, Jian Jin¹, Xiao-Hua Zhang⁴

Affiliations

¹ Frontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences, Ocean University of China, 5 Yushan Road, Qingdao 266003, China.
² Frontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences, Ocean University of China, 5 Yushan Road, Qingdao 266003, China; Laboratory for Marine Ecology and Environmental Science, Laoshan Laboratory, Qingdao 266237, China; Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China.
³ Laboratory for Marine Ecology and Environmental Science, Laoshan Laboratory, Qingdao 266237, China; Key Laboratory of Marine Chemistry Theory and Technology, Ministry of Education, Ocean University of China, Qingdao 266100, China.
⁴ Frontiers Science Center for Deep Ocean Multispheres and Earth System, and College of Marine Life Sciences, Ocean University of China, 5 Yushan Road, Qingdao 266003, China; Laboratory for Marine Ecology and Environmental Science, Laoshan Laboratory, Qingdao 266237, China; Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao 266003, China. Electronic address: xhzhang@ouc.edu.cn.

PMID: 37979570
DOI: 10.1016/j.watres.2023.120849

Abstract

Microbial community dynamics directly determine their ecosystem functioning. Despite the well-known annual recurrence pattern, little is known how different lifestyles affect the temporal variation and how community assembly mechanisms change over different temporal scales. Here, through a high-resolution observation of size fractionated samples over 60 consecutive weeks, we investigate the distinction in weekly distribution pattern and assembly mechanism between free-living (FL) and particle-associated (PA) communities in highly dynamic coastal environments. A clear pattern of annual recurrence was observed, which was more pronounced in FL compared to PA, resulting in higher temporal specificity in the former samples. Both the two size fractions displayed significant temporal distance-decay patterns, yet the PA community showed a higher magnitude of community variation between adjacent weeks, likely caused by sudden, drastic and long-lived blooms of heterotrophic bacteria. Generally, determinism (environmental selection) had a greater effect on the community assembly than stochasticity (random birth, death, and dispersal events), with significant contributions from temperature and inorganic nutrients. However, a clear shift in the temporal assembly pattern was observed, transitioning from a prevalence of stochastic processes driving short-term (within a month) fluctuations to a dominance of deterministic processes over longer time intervals. Between adjacent weeks, stochasticity was more important in the community assembly of PA than FL. This study revealed that stochastic processes can lead to rapid, dramatic and irregular PA community fluctuations, indicating weak resistance and resilience to disturbances, which considering the role of PA microbes in carbon processing would significantly affect the coastal carbon cycle. Our results provided a new insight into the microbial community assembly mechanisms in the temporal dimension.

Keywords: Assembly process; Coastal water; Microbial community; Particle-associated; Time series.

MeSH terms

Bacteria
Microbiota*
Seawater / microbiology
Stochastic Processes